growth and survival of hatchling saltwater crocodiles (crocodylus porosus…44878/thesis_cdu... ·...

Growth and survival of hatchling saltwater crocodiles

(Crocodylus porosus) in captivity: the role of agonistic

and thermal behaviour

Matthew Lindsay Brien

BSc. Hons. (University of Queensland)

Submitted in fulfilment of the requirements for the degree of Doctor of

Philosophy

Research Institute for the Environment and Livelihoods

Charles Darwin University

March 2015

ii

Hatchling saltwater crocodile (Crocodylus porosus) emerges from egg (photo credit:

Jemeema Brien).

iii

Declaration

This work contains no material which has been accepted for the award of any other

degree or diploma in any university or other tertiary institution and, to the best of my

knowledge and belief, contains no material previously published or written by another

person, except where due reference has been made in the text.

I give consent to this copy of my thesis, when deposited in the University Library,

being made available for loan and photocopying online via the University’s Open

Access repository eSpace.

Matthew L Brien

September 2014

iv

Acknowledgements

First and foremost, I would like to thank my wife, Jemeema, and my family for their

amazing love, support, and understanding throughout the last few years. It is a rare

and amazing thing to have a partner that not only shares the same love and passion for

all things scaly, but has also willingly been by my side in the bug infested swamps

and marshes all over the world for the best part of 10 years. Her knowledge and

understanding of crocodiles, and in particular hatchling saltwater crocodiles, has been

invaluable during this research. I have been very fortunate to also have a family that,

even though they may find it hard at times to comprehend what it is I do, why, and for

such little money, they have always supported me unconditionally in pursuit of my

dreams. My Nan died shortly before I finished my thesis, but I know she was proud.

This research would not have been possible without the logistical, technical, financial,

and intellectual support of Grahame Webb and Charlie Manolis through Wildlife

Management International (WMI). I have benefited from their amazing generosity

and support of student research, and have witnessed first hand the vast number of

students throughout the world who they have also helped, often at a financial cost to

WMI. I am greatly appreciative, and it is this generosity and insistence on high quality

research that I will take with me. I am also grateful to all WMI staff that have assisted

and supported with the research in various capacities over the years. These include

John Pomeroy, Steve Coulson, Dave Ottway, Tate Chambers, and the many hatchery

staff: Sally Sibley, Tanya Bradley, Jodi Cox, Sharon Harlock, and Olivia Plume. My

supervisors have been a great source of knowledge, guidance, and support throughout,

and have been incredibly generous with their time and efforts. To me they have been

v

the perfect balance of the practical and dependable (Keith Christian), innovative and

inspiring (Grahame Webb), statistical and clinical (Keith McGuinness), and the

crocodile behavioural guru (Jeff Lang). It has been a privilege and an honour to work

with all four. However, I am fortunate to have had someone like Keith (Christian) as

my primary supervisor. His calm and composed nature often belies his brilliance, and

he has been a great source of guidance, balance and support throughout. I would like

to make special mention of Chris Gienger, who as a recently graduated PhD student

and post-doctoral at Charles Darwin University, provided critical mentorship,

guidance and advice early on that I am indebted to. I would also like to thank the two

Dutch veterinary students, Elize and Evelyn, for their help, and Steve Garnett for

advice and guidance early on. Cathy Shilton from Berrimah Veterinary labs is

brilliant, and I enjoyed working with her on the Valium and Tryptophan chapter.

Funding through WMI from the Rural Industries Research and Development

Corporation is gratefully acknowledged, as is the funding provided through

Holsworth Wildlife Research Endowment (ANZ Trustees Foundation), Northern

Territory Research and Innovation Board student grants, IUCN Crocodile Specialist

Group student grant, and Charles Darwin University student grants. Last but not least,

I will be forever grateful to the object of my passion and inspiration, the crocodile.

But for crocodiles, I would never have considered myself capable of doing Honours,

much less a PhD.

vi

Abstract

Agonistic and thermal behaviour was studied in hatchling Crocodylus porosus under

captive conditions using CCTV cameras. The results guided the design of experiments

aimed at improving growth and survival of this species in captivity. C. porosus are

born with a repertoire of 16 distinctive agonistic behaviours, and most interactions

occur in the morning and evening in open, shallow water. There are clutch-specific

differences in the frequency of agonistic interactions, and older hatchlings display

fewer behaviours based on dominance status. A comparison of eight crocodilian

species revealed differences in behaviours displayed and the level of conspecific

tolerance, with C. porosus being the most aggressive. Hatchling C. porosus preferred

body temperatures (Tbs) between 29.4ºC and 32.6ºC, and the mean (30.9±2.3ºC SD)

was not influenced by social situation or feeding status. During the day, hatchlings

had higher Tbs and were less active than at night. Growth of C. porosus during the

first 24 days can be used to predict ‘failure to thrive’ (FTT) affliction up to 300 days.

Hatchlings fed short chopped meat had higher growth than those fed standard mince

or long chopped meat. Although visual barriers and deeper water reduced agonistic

behaviour among hatchlings, these factors did not result in improved growth.

Hatchling growth was highest at a density of 6.7/m2, and was lower at higher

densities. The frequency of agonistic interactions was higher at lower densities

(3.3/m2; 6.7/m

2) than at higher densities (13.3/m

2; 20.0/m

2). Although hatchlings

given Valium in their food had fewer agonistic interactions, they had reduced growth.

Hatchlings raised under constant warm temperatures (32-34ºC), a gradient of

temperatures, or warmer night time temperatures had higher growth than hatchlings

vii

with warm temperatures during the day only. Hatchlings afflicted with FTT and

placed in a semi-natural enclosure had almost double the growth of those in standard

raising pens.

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Publications arising from this Thesis

Each chapter has been formatted as a journal article, so there is a lot of repetition

throughout the thesis. Sections of the thesis that were published in peer reviewed

journals during the candidature (2.1, 3.1, 3.2, 3.3, 4.1, and 5.1) are formatted

according to the journal’s specifications. For each published manuscript, supervisors

were included as co-authors. Chris Gienger was also a co-author on two papers (2.1,

5.1). All co-authors consented to the publication of these manuscripts in each of the

journals, as well as in this thesis. Chapters that had not been submitted for publication

prior to the submission of this thesis are formatted in the same way.

List of publications:

Brien, M.L., Webb, G.J., Gienger, C.M., Lang, J.W., Christian, K.A., 2012.

Thermal preferences of hatchling saltwater crocodiles (Crocodylus porosus) in

response to time of day, social aggregation and feeding. Journal of Thermal Biology

37, 625–630.

(Chapter 4.)

Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian, K.A., 2013.

Born to be bad: agonistic behaviour in hatchling saltwater crocodiles (Crocodylus

porosus). Behaviour 150: 737–762.

(Chapter 3.1)

ix

Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian, K.A. 2013.

Intra- and interspecific agonistic behaviour in hatchling Australian freshwater

crocodiles (Crocodylus johnstoni) and saltwater crocodiles (Crocodylus porosus).

Australian Journal of Zoology 61: 196-205. Won ‘Best Student Paper Award 2013’

with the Australian Journal of Zoology.

(Chapter 3.2)

Brien, M.L., Lang, J.W., Webb, G.W., Stevenson, C., Christian, K.A. 2013. The

good, the bad, and the ugly: agonistic behaviour in juvenile crocodilians. PloS one

8: DOI: 10.1371/journal.pone.0080872.

(Chapter 3.3)

Brien, M.L., Webb, G.J., McGuinness, K.A., Christian, K.A. 2014. The relationship

between early growth and survival of hatchling saltwater crocodiles (Crocodylus

porosus) in captivity. PloS ONE 9: e100276. doi:10.1371/journal.pone.0100276.

(Chapter 2.1)

Brien, M.L., Gienger, C.M., Webb, G.J., McGuinness, K.A., Christian, K.A., 2014.

Out of sight or in too deep: effect of visual barriers and water depth on agonistic

behaviour and growth in hatchling saltwater crocodiles (Crocodylus porosus).

Applied Animal Behaviour Science – in press.

(Chapter 5.1)

In each publication, Grahame Webb and Keith Christian were primarily involved in

x

developing study design and methodology, as well as reviewing early drafts of the

manuscript. Keith McGuinness reviewed experimental design, provided statistical

advice and ran some of the analyses, and also reviewed early drafts. Jeff Lang and

Chris Gienger provided advice on study design and reviewed early drafts of the

manuscripts that they co-authored.

xi

Table of Contents

CHAPTER 1. GENERAL INTRODUCTION ....................................... 1

Conservation and management of C. porosus ...................................................................................... 1

Survivorship and population dynamics of C. porosus ......................................................................... 2

Crocodylus porosus in the Northern Territory ..................................................................................... 9

Failure to thrive syndrome .................................................................................................................. 10

Addressing FTT: factors that may influence growth and survivorship of hatchling C. porosus ... 14

Limitations of previous research ......................................................................................................... 20

Intended aims and goals of this thesis ................................................................................................. 22

Literature Cited .................................................................................................................................... 24

CHAPTER 2. THE RELATIONSHIP BETWEEN EARLY

GROWTH AND SURVIVAL OF HATCHLING SALTWATER

CROCODILES (CROCODYLUS POROSUS) IN CAPTIVITY ......... 39

Abstract ................................................................................................................................................. 39

Introduction .......................................................................................................................................... 40

Materials and Methods ........................................................................................................................ 42

Results ................................................................................................................................................... 47

Discussion .............................................................................................................................................. 61

Acknowledgements ............................................................................................................................... 65

References ............................................................................................................................................. 66

CHAPTER 3.1. BORN TO BE BAD: AGONISTIC BEHAVIOUR IN

HATCHLING SALTWATER CROCODILES (CROCODYLUS

POROSUS) ............................................................................................... 79

Summary ............................................................................................................................................... 79

Introduction .......................................................................................................................................... 80

Materials and methods ......................................................................................................................... 83

Results ................................................................................................................................................... 89

Discussion ............................................................................................................................................ 100

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Acknowledgements ............................................................................................................................. 108

References ........................................................................................................................................... 108

CHAPTER 3.2. INTRA- AND INTERSPECIFIC AGONISTIC

BEHAVIOUR IN HATCHLING AUSTRALIAN FRESHWATER

CROCODILES (CROCODYLUS JOHNSTONI) AND SALTWATER

CROCODILES (CROCODYLUS POROSUS) .................................... 119

Abstract ............................................................................................................................................... 119

Introduction ........................................................................................................................................ 120

Materials and methods ....................................................................................................................... 122

Results ................................................................................................................................................. 127

Discussion ............................................................................................................................................ 138


References ........................................................................................................................................... 148

CHAPTER 3.3. THE GOOD, THE BAD, AND THE UGLY:

AGONISTIC BEHAVIOUR IN JUVENILE CROCODILIANS .... 157

Abstract ............................................................................................................................................... 157

Introduction ........................................................................................................................................ 158

Materials and Methods ...................................................................................................................... 160

Results ................................................................................................................................................. 168

Discussion ............................................................................................................................................ 190


References ........................................................................................................................................... 205

CHAPTER 4. THERMAL PREFERENCES OF HATCHLING

SALTWATER CROCODILES (CROCODYLUS POROSUS) IN

RESPONSE TO TIME OF DAY, SOCIAL AGGREGATION AND

FEEDING .............................................................................................. 217

Abstract ............................................................................................................................................... 217

1. Introduction .................................................................................................................................... 218

2. Materials and Methods .................................................................................................................. 221

3. Results ............................................................................................................................................. 225

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4. Discussion ........................................................................................................................................ 233


References ........................................................................................................................................... 238

CHAPTER 5.1. OUT OF SIGHT OR IN TOO DEEP: EFFECT OF

VISUAL BARRIERS AND WATER DEPTH ON AGONISTIC

BEHAVIOUR AND GROWTH IN HATCHLING SALTWATER

CROCODILES (CROCODYLUS POROSUS) .................................... 246

Abstract ............................................................................................................................................... 246

1. Introduction .................................................................................................................................... 247

2. Animals, materials, and methods .................................................................................................. 250

3. Results ............................................................................................................................................. 257

4. Discussion ........................................................................................................................................ 260

5. Conclusion ....................................................................................................................................... 263


References ........................................................................................................................................... 264

CHAPTER 5.2. EFFECT OF DENSITY ON GROWTH,

AGONISTIC BEHAVIOUR, AND ACTIVITY IN HATCHLING

SALTWATER CROCODILES (CROCODYLUS POROSUS) ......... 268

Abstract ............................................................................................................................................... 268

Introduction ........................................................................................................................................ 269

Methods ............................................................................................................................................... 271

Results ................................................................................................................................................. 275

Discussion ............................................................................................................................................ 282


Literature Cited .................................................................................................................................. 289

CHAPTER 5.3. FACTORS AFFECTING INITIAL GROWTH

RATES OF CAPTIVE SALTWATER CROCODILES

(CROCODYLUS POROSUS) HATCHLINGS IN CAPTIVITY:

FOOD FORM AND TEMPERATURE CYCLE ............................... 298

Abstract ............................................................................................................................................... 298

xiv

Introduction ........................................................................................................................................ 299

Methods ............................................................................................................................................... 302

Results ................................................................................................................................................. 307

Discussion ............................................................................................................................................ 313



CHAPTER 5.4. USE OF DIAZEPAM AND TRYPTOPHAN TO

REDUCE STRESS AND INCREASE GROWTH AND SURVIVAL

OF HATCHLING SALTWATER CROCODILES (CROCODYLUS

POROSUS) IN CAPTIVITY ................................................................ 327

Abstract ............................................................................................................................................... 327

Introduction ........................................................................................................................................ 328

Methods ............................................................................................................................................... 330

Results ................................................................................................................................................. 335

Discussion ............................................................................................................................................ 341



CHAPTER 6. IMPROVING GROWTH AND SURVIVAL IN

HATCHLING C. POROSUS: SUMMARY, OUTDOOR

ENCLOSURES, AND CONCLUSIONS ............................................ 352

Agonistic behaviour ............................................................................................................................ 352

Thermal behaviour ............................................................................................................................. 354

Growth and survival........................................................................................................................... 355

Understanding agonistic behaviour .................................................................................................. 356

Optimal thermal regime ..................................................................................................................... 358

The raising environment: a case study ............................................................................................. 359

Methods ............................................................................................................................................... 360

Results ................................................................................................................................................. 362

Discussion ............................................................................................................................................ 366

Conclusions and Recommendations .................................................................................................. 368

xv



1

Chapter 1. General Introduction

Conservation and management of C. porosus

Saltwater crocodiles (Crocodylus porosus) are one of the largest and most widely

distributed of living crocodilians, ranging from Sri Lanka and India in the north-west,

across south-east Asia to the Phillipines and some Pacific Islands in the north east,

and down through Indonesia, Papua New Guinea and Australia to the south (Ross

1998; Webb et al. 2010). The skins of C. porosus are also the most commercially

valuable of any of the 23 species of extant crocodilians, because they have relatively

small scales and no osteoderms in the scales of the ventral skin, the ‘belly’ skin,

which is the most prized for high quality fashion leather (Webb and Manolis 1989;

Fuchs 2006).

Historically (<1960s), all wild C. porosus populations were greatly reduced through

eradication as pests, particularly as predators on people and livestock, loss of habitat

and through hunting for skins (Ross 1998; Webb et al. 2010). Throughout much of the

former range of C. porosus, wild populations are either highly depleted, extinct, or

represented by small remnants in some protected areas (Ross 1998; Webb et al. 2010).

In contrast, countries such as Australia, Brunei, Papua New Guinea, Sarawak, Sabah,

and the Solomon Islands have implemented successful management programs to

encourage wild populations to recover (Webb et al. 2010).

National priorities with C. porosus since the 1960’s have varied from country to

2

country (Ross 1998). However, it has proven virtually impossible to rebuild wild

populations of C. porosus in areas with high density human populations that are

vulnerable to crocodile attacks because people use rivers and wetlands continually

(Ross 1998; Webb et al. 2010).

Crocodile farms and ranches are intimately linked to the success of programs in parts

of Australia, Indonesia and Papua New Guinea, where the commercial benefits

derived from using wild C. porosus populations, provide incentives for people to

tolerate large and expanding wild populations of C. porosus (Hutton and Webb 1992;

Webb et al. 2010). Underlying such programs are various assumptions concerning

how the population dynamics of wild C. porosus populations will respond to

interventions (Webb and Smith 1987).

Survivorship and population dynamics of C. porosus

The balance of population dynamics that determine whether a population increases,

decreases, or remains stable is dependent on rates of reproduction, mortality,

immigration and emigration (Hutchinson 1978). The same is true in captive

populations, but here the parameters are largely controlled to get particular outcomes.

The success or failure of both wild and captive populations of C. porous is based on

assumptions about population dynamics, with age-specific survival rates being of

critical importance (Webb and Smith 1987; Hutton and Webb 1992). Indeed, the

whole theoretical basis of ranching programs in Australia, Indonesia and Papua New

3

Guinea is based on assumptions about age-specific survival rates.

Rates of survival are known to vary within and among species and populations

depending on habitat, food, weather, and the size structure of the population (Webb

and Smith 1987). Regardless, survival rates for C. porosus are typically lowest in the

early life stages (eggs and hatchlings), when predators and environmental problems

are greatest, and increase with increasing size and age (Webb et al. 1983). However, if

eggs and juveniles are collected and raised on farms, many of the animals that would

be destined to die in the wild are assumed to have ‘high survival rates’ in captivity

(Webb and Smith 1987; Hutton and Webb 1992). The ecological impact of collecting

eggs and juveniles should thus theoretically be minimal, and if necessary, can be

compensated for by a release back to the wild of some captive raised juveniles (Elsey

et al. 1992).

Eggs

Female C. porosus build mound nests primarily out of vegetation near water, which

they are known to actively and aggressively defend in the wild and in captivity (Webb

et al. 1977; 1983). Egg-laying occurs mainly during the wet season, with low egg

survivorship (as low as 25% in some areas) in the wild due to flooding (Webb et al.

1977). Predation on C. porosus nests, outside of ranching programs, is considered to

be very low (<2%) (Webb et al. 1984; 1987). In captivity, populations of C. porosus

experience high egg survivorship (80-95%) from viable eggs either ranched from the

wild or collected from captive bred stock, and incubated artificially (Hutton and Webb

4

1992).

Previous studies suggest that genetics and the nature of embryonic development are

two of the most important factors determining overall growth and survival of

crocodiles, with differences in the performance of individuals often directly related to

the clutch of origin and the environmental conditions experienced during incubation

(Webb and Cooper-Preston 1989; Deeming and Ferguson 2009). This is referred to as

the ‘clutch affect’, and while this influence can sometimes be physically apparent, in

the form of abnormalities, degree of yolk absorption, sex determination, and size at

hatching, it can also have important physiological and behavioural implications for

survival that are less obvious and still poorly understood (Webb et al. 1987; Webb and

Cooper-Preston 1989; Riese 1991). For example, parameters such as dietary and

thermal preferences, along with social tolerance may already be determined before

hatching (Webb and Cooper-Preston 1989; Sneddon et al. 2000). The ‘clutch’ affect

among hatchling crocodilians is so strong that the results of many studies have been

compromised because they have failed to recognise and adjust for this affect when

designing experiments.

Temperature during incubation is critical in determining the rate of embryonic

development, degree of yolk absorption and size at hatching (Ferguson and Joanen

1982; 1983; Webb et al. 1987). Although the size of an individual at hatching is

determined by the size of the egg (Webb et al. 1983), it is unknown whether larger

body size in hatchling crocodilians is related to increased growth and survival (Webb

and Cooper-Preston 1989) as is the case with a number of other reptiles (Congdon and

5

Gibbons 1985; Sinervo 1990; Stearns 1992; Janzen 1993).

For C. porosus, ideal conditions for artificial incubation are considered to be a

constant 32ºC and 90-95% relative humidity, which result in mostly male (85%)

hatchlings emerging after 80 days (Webb and Cooper-Preston 1989; Richardson et al.

2002). At temperatures higher or lower than 32ºC, the sex ratio will be split between

males and females and overall survival is generally lower (Webb and Cooper-Preston

1989; Whitehead et al. 1989). At higher temperatures (>32ºC), hatchling C. porosus

develop more rapidly and show trends toward neotony, where they hasten

development and tend to hatch with small body size and abundant yolk (Webb and

Cooper-Preston 1989; Whitehead et al. 1989). At lower temperatures (<32ºC)

incubation times are extended, and more of the yolk is used in embryonic growth,

although at very low temperatures (~28ºC), development is so compromised that

internalisation of yolk itself becomes problematic (Webb and Cooper-Preston 1989;

Whitehead et al. 1989). Once hatched, individual C. porosus have higher growth rates

when raised at a temperature similar to that experienced during incubation (Webb and

Cooper-Preston 1989).

Hatchlings

After the female has uncovered the nest and transported the hatchlings to the water,

she usually remains within the vicinity of the clutch anywhere from 1-8 weeks (Webb

et al. 1977; 1983). Whether survival of hatchling C. porosus is dependent upon the

degree of protection provided by the female and if it decreases after the crèche of

6

hatchlings disperses is not known. It is possible that female C. porosus may be

important in keeping the crèche together (Webb et al. 1977; Magnusson 1979) and in

the provisioning of food, as has been demonstrated for other species of crocodilians in

captivity (Whitaker 2007).

In the wild, approximately 54% of hatchling C. porosus successfully survive to one

year, with most mortality through predation (Webb et al. 1987). There are a wide

range of species (bird, fish, crustacean, reptile) reported to consume hatchling C.

porosus and this is considered to be the primary cause of mortality in the wild.

Species that are believed to predate hatchling C. porosus in Australia include goannas

(eg. Varanus indicus), fish (eg. Lates calcarifer, Scleropages leichardti), sharks

(Glyphis spp.), kites (eg. Milvus and Haliastur spp.), sea eagles (Haliaeetus

leucogaster), herons (eg. Nycticorax caledonicus), turtles (eg. Chelonea rugosa),

crabs (Scylla serrata), and larger C. porosus (Messel and Vorlicek 1989; Webb and

Manolis 1998; Somaweera et al. 2013). While it is widely accepted that predation is a

significant cause of mortality among hatchling C. porosus, actual predation events are

rarely seen due to the cryptic and aquatic nature of hatchlings and a number of the

species that prey upon them (Magnusson 1984). In captivity, predation is largely

controlled, and in most cases is non-existent for hatchling C. porosus raised in

appropriate facilities.

For C. porosus, hatchling survivorship to one-year-of-age in the wild is correlated

with the total number of hatchlings in the population (Webb and Manolis 2001).

Lower survival rates have been reported in years when more hatchlings are produced

7

in at least some rivers (Messel et al. 1981; Webb and Manolis 2001). The number of

adults in the population appears to have limited influence on hatchling survivorship,

suggesting cannibalism may be of minor significance with this life stage (Magnusson

1984; Webb and Manolis 2001). However, cannabilism is considered to have a

significant influence on survivorship in several other species of crocodilian (Cott

1961; Staton and Dixon 1975; Rootes and Chabreck 1993; Delaney et al. 2011;

Somaweera et al. 2013). Hatchling survivorship to one year in captivity is

considerably higher, with the majority of mortalities due to runtism or a failure to

thrive (FTT) syndrome (Mayer 1998; Isberg et al. 2009).

Sub-adults

After the first year, crocodiles are larger and the threat of predation is reduced

resulting in higher survivorship (up to 70%) between one and two years of age in the

wild (Webb et al. 1984; 1987). Between two and four years of age, survival depends

on adult density. In wild populations with fewer adults, average survival from 2-4

years is around 66%, while in populations with more adults, survival can be as low as

30% (Messel et al. 1981; Webb et al. 1984; 1987). In comparison, rates of survival

after one year of age in captivity are typically greater than 95% until slaughter at 3-5

years of age (Mayer 1998; Isberg et al. 2009).

In the wild, cannibalism of juveniles between 1 and 2 years of age is highly correlated

with the number of larger crocodiles present (>2m total length), suggesting

cannibalism may become more important with size (Messel et al. 1981; Webb and

8

Manolis 2001). Beyond two years of age, cannibalism and social exclusion (perhaps

linked with lower survival rates) increase in importance (Messel et al. 1981; Webb

and Manolis 2001).

Adults

Adult C. porosus have few predators other than humans and other crocodiles (Messel

et al. 1981; Webb and Manolis 2001). Once individuals reach adulthood survivorship

is generally high, at least for females. However, males are known to kill rivals in

disputes over territories and mates during the breeding season (Webb and Manolis

2001).

Population dynamics

Knowledge of survival rates is thus critical for understanding population dynamics

when trying to predict how a wild population of C. porosus is likely to respond to

management interventions, or explain how they have responded where interventions

have already taken place (Webb and Smith 1987; Hutton and Webb 1992). Survival

rates, particularly amongst hatchlings, are also important for understanding the

dynamics of captive populations of C. porosus on farms and ranches, and the

biological and commercial viability of such enterprises (Webb and Smith 1987;

Hutton and Webb 1992).

9

Crocodylus porosus in the Northern Territory

Although two species of crocodilian occur in northern Australia, C. porosus and the

freshwater crocodile (Crocodylus johnstoni), farming is largely restricted to C.

porosus due to the slow growing nature and smaller size of C. johnstoni, and the

poorer quality skin it produces (Hutton and Webb 1992; Webb et al. 2010). While

farming of C. porosus is restricted to captive breeding in Queensland, the industry in

the Northern Territory and Western Australia is now based on both captive breeding

and a ranching program, in which eggs are collected from the wild and incubated

artificially (Letnic 2004; Webb et al. 2010). Ranched eggs from the Northern

Territory are also used to stock farms in Queensland (Webb et al. 2010).

In the Northern Territory, where severely depleted wild populations of C. porosus

were protected in 1971, the wild populations have now almost fully recovered

(Fukuda et al. 2011). Current management programs for C. porosus allow strictly

controlled commercial use, through both ranching of wild eggs and captive breeding

(Letnic 2004; Webb et al. 2010). Eggs are artificially incubated and the resultant

hatchlings raised on crocodile farms (Letnic 2004; Webb et al. 2010). This program

is one mechanism through which C. porosus have been made economically beneficial

to the people of the Northern Territory, and so between 1971 and 2010 they have

tolerated a 20 times increase in C. porosus abundance and a 100 times increase in C.

porosus biomass (Fukuda et al. 2011).

In commercial captive raising facilities within the Northern Territory, average

10

survival rates of C. porosus between hatching and one-year-of-age are generally

reported to be 80-90% (Isberg et al. 2004; Department of Resources - DoR).

However, this figure is based on self reporting by farms and a mandatory hatchling

audit undertaken by the DoR each year during October-November. As C. porosus

hatch out late December through early July, with the majority between February and

April, this survival rate is for animals ranging between 3-10 months old. A study on

one farm reported that only 51% of hatchlings produced from captive stock survived

to 400 days old (Isberg et al. 2006; 2009). Therefore, the figure of 80-90% annual

survivorship of hatchling C. porosus to one year is considered an overestimate.

Regardless, these survival rates are still significantly lower than the 95-99%

survivorship to one-year-of-age reported for American alligators (Alligator

mississippiensis) hatched in artificial incubators and raised under similar conditions

(Joanen and McNease 1976).

Failure to thrive syndrome

In captive raising facilities for C. porosus, losses due to predation are rarely

encountered. The mortality that does occur appears to be the consequence of a ‘failure

to thrive syndrome (FTT)’ or ‘runtism’ (Mayer 1998; Isberg et al. 2004). For reasons

that are not clear, 15-40% of C. porosus hatchlings eat and grow little relative to

others, including siblings, and become vulnerable to mortality through reduced

immunity to disease and/or voluntary starvation (Onions 1987; Webb et al. 1987;

Mayer 1998; Isberg et al. 2009). These individuals become emaciated and usually die

between 70-200 days, or need to be culled (Huchzermeyer 2003; Isberg et al. 2009).

11

Whether or not wild C. porosus hatchlings are as afflicted by FTT as their captive

raised counterparts is unclear. In the wild, individual growth rates are highly variable

(Webb et al. 1978), yet amongst hatchlings caught or sighted in surveys, FTT or

anorexic animals are rarely reported (Webb pers. com.). However, as hatchlings in the

wild suffering from FTT would be more susceptible to predation, accurately

determining its prevalence would not be possible. Also, hatchlings of other

crocodilians (A. mississippiensis, C. acutus) suffering from FTT have been observed

in the wild.

FTT is the leading cause of hatchling C. porosus mortality up to one year old on

Australian farms each year (Hibberd et al. 1996; Mayer 1998; Isberg et al. 2009).

Total losses attributable to FTT are probably higher, with some animals that suffer

from FTT often surviving until the second year before they either die or need to be

culled due to stunted growth (Isberg et al. 2009). There are no known infectious

diseases that cause FTT, although animals suffering FTT usually succumb to

opportunistic infections due to their compromised state (Isberg et al. 2009).

Although FTT may be more prevalent in the wild than currently accepted, it is

common in captivity, which clearly constrains production efficiency on farms, and

equally important, confounds the ability to test and experiment (Mayer 1998; Isberg et

al. 2009). One consequence of FTT is that the size distribution of hatchlings in

captivity rapidly becomes bimodal which increases variability. A problem

exacerbated by the experimental treatment resulting in the largest hatchlings, also

12

providing the smallest ones (the largest number of animals with FTT).

FTT in captive raised C. porosus may be a product of the raising environment and

raising protocols used for hatchlings (Hutton and Webb 1992; Buenviaje 1994).

Although pens and procedures vary from farm to farm, and are continually being

adapted and modified by crocodile farmers, they all seem to be variants of the same

basic approach to raising based on the same assumptions – the C. porosus raising

paradigm (Hutton and Webb 1992).

The possibility that this raising paradigm, instigated some 30 years ago, is

fundamentally compromised for C. porosus hatchlings cannot be rejected. When

crocodile farming started in Australia, particularly during the 1970’s, survival and

growth rates of hatchlings were problematic (Garnett and Murray 1986; Onions 1987;

Webb et al. 1987; Mayer 1998). The same occurred with Nile crocodiles (Crocodylus

niloticus) when farming started (Hutton and Webb 1992). In both cases, it was

considered that ‘outdoor’ pens would provide a more natural raising environment, and

that problems could be overcome by trial, error, innovation and research in captivity

(Riese 1995; Mayer 1998; Davis 2001)

However, the raising paradigm implemented with American alligators (Alligator

mississippiensis) was based on ‘indoor’ raising in controlled environments

(particularly temperature) and the results in terms of survival and growth rates were

by comparison exceptionally good (Joanen and McNease 1976). This led to a shift

towards controlled environment raising of both C. porosus and C. niloticus, which

13

improved both survival and growth rates (Hutton and Webb 1992). However, with C.

porosus at least, the problem of FTT remained. At that time the possibility of species-

specific traits affecting the ideal raising environment had not been explored. Although

little information exists, substantially higher rates of growth and survival to one year

of age have been reported for A. mississippiensis when raised under identical

conditions to C. porosus (Webb et al. 1994).

In any overview, the raising strategies implemented for C. porosus are the result of

adaptive management: corrected error to corrected error. The starting point was not

based on a sound understanding of how hatchling C. porosus behave, feed, grow,

thermoregulate or function because this information was not available at the time. Nor

did it take into account the possibility that significant species-specific traits may be

involved: technologies that work well with one species may not be automatically

transferable to others.

That FTT is common in captive raised crocodiles suggests that the general raising

environment used for C. porosus may be inadequate (Onions 1987; Hutton and Webb

1992). This crocodilian has long been regarded as a species least tolerant of

conspecifics (Lang 1987), so it seems possible that social behaviour may be

implicated in FTT. The possibility that behavioural ‘bullying’ promotes fast growth

rates in dominant hatchlings, and FTT in sub-dominant ones, has rarely been

considered because social interactions such as this in the first few weeks have not

been reported. Information on hatchling C. porosus in the wild may provide valuable

insights into the causes of FTT and potential options for managing it in captivity.

14

Addressing FTT: factors that may influence growth and survivorship of

hatchling C. porosus

Along with genetics, embryonic development, parental care, and predation, other

factors that can potentially influence survival of hatchling C. porosus in both the wild

and captivity include diet, movement and habitat use, thermoregulation, social

dynamics, and size and age. The following sections examine what is currently known

about hatchling C. porosus in the wild and in captivity. Information from the wild is

critical to understanding hatchling C. porosus survivorship and may provide clues to

improving captive management and therefore reducing the incidence of FTT.

Diet

Hatchling C. porosus in the wild feed intermittently on a diet of small crustaceans

(predominantly crabs), insects, and occasionally fish, usually captured in shallow

water near the land water interface during the night (Taylor 1979; Webb et al. 1991).

Wild hatchling C. porosus appear to be far more efficient at converting food in to

increased body mass, compared with individuals raised in captivity (Garnett and

Murray 1986; Webb et al. 1991). In general, hatchling C. porosus are attracted to

movement and readily consume live food (Webb et al. 1991; Hutton and Webb 1992).

However, while providing live food to hatchlings in captivity is rarely economically

practical (Hutton and Webb 1992), if the shape or form of the food is too different

from that of prey then it may negatively impact consumption and result in FTT.

15

A number of studies have been dedicated to dietary preference and feeding regimes of

hatchling C. porosus in captivity (Garnett and Murray 1986; Mayer et al. 1997; Davis

2001). Hatchling C. porosus are typically fed a red meat based diet in combination

with multivitamin and calcium supplements five to six days a week (Hutton and Webb

1992; Mayer et al. 1997; Davis 2001). This regime achieves superior growth for the

large majority of hatchling C. porosus (80-85%) compared to diets based on fish, or

pelletized food (Hutton and Webb 1992). However, there appears to be clutch and

individual specific dietary preferences, and so providing a mixture of different protein

sources may be important for achieving higher rates of growth and survival (Garnett

and Murray 1986; Manolis et al. 1990; Hutton and Webb 1992).

It has been argued that the odor of a food source may affect consumption, and that

hatchling C. porosus may be inherently wary of piles of meat, as in the wild this

would generally attract larger crocodiles and other scavengers that could feed on

small hatchlings (Manolis et al. 1990). In comparison, alligators achieve high rates of

growth and survival (>90%) when raised on any number of different food types,

including red meat, fish or pelletized food containing vegetable protein (Staton et al.

1990; Hutton and Webb 1992). Alligators are also far more adaptable when it comes

to changing between different feed types (Hutton and Webb 1992).

Movement and habitat use

Despite differences between habitats, hatchling C. porosus in the wild make few if

16

any large scale movements during the first year, with individuals often found within

several kilometres of the nest site (Webb and Messel 1978; Webb et al. 1978).

Hatchling crocodiles spend the majority of the day hidden in cover among vegetation,

branches and logs near the water’s edge (Platt and Thorbjarnarson 2000; Mazzotti et

al. 2007). This cryptic behaviour enables them to not only avoid predators but may

also allow them to thermo-regulate more effectively (Bolton 1990; Pooley 1990;

Riese 1991). It is unknown how movement patterns and habitat use change in

response to different weather patterns and season. In captivity, hatchling C. porosus

that are not provided with some form of shelter tend to pile on top of each other and

grow less, compared with those in which shelter is provided (Riese 1991; Mayer

1998; Davis 2001). Hatchling C. porosus are prey to a wide range of predators and so

the amount and type of cover provided could have important implications for FTT.

Thermal relations

Crocodilians are largely dependent upon their environment for heat, and have the

ability to warm up twice as fast as they can cool (Boland and Bell 1980; Lang 1987;

Hutton and Webb 1992). However, the rate of heat exchange with the environment is

directly related to the mass of the individual, with adults heating and cooling at a

slower rate than hatchlings due to greater thermal inertia (Lang 1979; Boland and Bell

1980). Hatchling crocodilians operate over a wider range of temperatures, achieving

preferred body temperatures through behavioural means (Lang 1987; Seebacher et al.

2003). However, the way in which they achieve preferred body temperatures differs

between species (Grigg and Seebacher 2000; Seebacher et al. 2003). While adults are

17

less sensitive to changes in temperature, smaller individuals are more adaptable to

prolonged shifts in environmental temperatures as they can utilize microhabitat to heat

and cool more rapidly (McNease and Joanen 1974; Pooley and Gans 1976).

Many species of crocodilian are maintained on farms at relatively constant high

temperatures (30-33ºC) (Hutton and Webb 1992). However, research suggests that

this approach may be inappropriate for optimal physiological functioning, due to the

need for individuals to vary their body temperature according to their physiological

state, with higher temperatures often sought after feeding or during illness, and lower

temperatures sought during fasting (Hutton and Webb 1992; Lang 1987). It is also

important to note that the large majority of reptile species raised in captivity are

provided with a range of thermal options within their enclosure, and that the

importance of this has long been recognised (Peaker 1969). Despite the success of

raising A. mississippiensis at constant high temperatures (30-33ºC), providing a

thermal gradient may be important for those species that inhabit year round warm

climates such as C. porosus that need the ability to cool down (Lang 1979; 1981;

1987).

Optimal temperatures (air and water) for hatchling C. porosus in captivity are

currently believed to be between 32ºC and 34ºC, with some studies reporting higher

rates of growth and survival at a constant 32ºC and others at 34ºC (Webb et al. 1990;

Mayer 1998; Davis 2001). Hatchling C. porosus maintained at either low (<26ºC) or

high temperatures (>34ºC) for long periods do poorly in terms of growth and survival

(Webb et al. 1990; Mayer 1998; Davis 2001), as do those in which only a localised

18

source of heat is provided (eg. heat lamp, hot water tap) that can not be accessed by

all individuals (Lang 1987; Webb and Manolis 1990; Riese 1991). As individuals get

larger, they are less reliant on an artificial source of heat and can be raised outdoors

under ambient conditions (Webb and Manolis 1990; Riese 1991).

There are almost no studies that have examined thermoregulatory behaviour of

hatchling C. porosus in the wild or in captivity. Lang (1981) provided some

information regarding thermal preference of hatchling C. novaeguineae in a natural

enclosure, and found that hatchlings selected higher temperatures (33.4-33.9ºC)

during the first two weeks than when they were between two and five weeks old

(31.8-32.2ºC), and that this was similar for hatchling C. porosus (Lang 1981). Just as

the provision of a varied diet may allow for clutch-specific dietary preferences,

providing a thermal gradient may allow for clutch-specific thermal preferences.

Understanding thermal relations of hatchling C. porosus in captive and wild settings is

important for improving captive management and reducing the incidence of FTT.

Social dynamics

Social interactions among crocodiles are known to have a strong influence over

almost all other behaviours (thermoregulatory, feeding, movement, habitat use etc)

(Lang 1987). As the natural inclination for young hatchlings of most species is to

group together in crèches, this will usually override normal thermoregulatory

behaviour (Lang 1987). Hatchlings in these groups will emit a high pitched call which

is believed to be important in keeping the crèche together, as well as to alert others of

19

danger (Magnusson 1979; Britton 2000). However, as hatchlings get older and grow

larger, dominance hierarchies begin to establish and individuals of low social status

can often be excluded from a resource (food, water, cover, etc.) (Riese 1991).

There is almost no information regarding the social interactions and behaviour of

hatchling C. porosus. In one study that examined hatchling C. porosus in the wild, a

recording of a hatchling played on the opposite bank to a crèche resulted in the whole

crèche relocating to the other side of the river (Magnusson 1979). However, whether

this grouping behaviour is simply for protection against predators, or whether there

are other social or thermoregulatory reasons that are important is unknown.

Hatchling C. porosus tend to disperse from the crèche after two months (Webb et al.

1977), while hatchling A. mississippiensis will remain together in some areas for up to

several years (Hunt 1982). The reason for earlier dispersal among hatchling C.

porosus may be due to an increasing intolerance of conspecifics (Webb and Messel

1978). However, it is unknown how early aggressive or dominant behaviours occur

and how important they are for survival.

In captivity, hatchling C. porosus appear to perform better at lower densities or group

sizes of around 10-15 individuals, with overcrowding (>30 individuals) causing lower

rates of growth and survival (Riese 1991; Webb et al. 1992; Mayer 1998). As

individuals grow, it is believed by some that larger group sizes may be preferable as it

may dilute the affect of social dominance (Mayer 1998). Regular sorting or grading of

animals by size is an effective strategy for breaking any dominance effects within a

20

group (Riese 1991). As with thermal relations, understanding social dynamics of

hatchling C. porosus in wild and captive settings is important for improving captive

management and reducing FTT.

Our understanding of these factors and how they interact to ultimately influence

survival of hatchling C. porosus remains poorly understood. As there is almost no

information regarding the social and thermal behaviour of hatchling C. porosus, this

research will provide new information that, combined with existing knowledge, will

be important for addressing the issues of survival and FTT.

Limitations of previous research

The dramatic increase in size that a hatchling crocodilian will go through to reach

adulthood, which in some cases can be an increase of more than five orders of

magnitude (Grigg and Seebacher 2000), is unmatched by most other vertebrate

species. As a result, hatchling and adult crocodilians have such different physiological

and behavioural requirements, that they could almost be considered separate species.

Hatchling crocodilians are small ‘prey’ species that group together, occupy sheltered

habitat, and shuffle between sun and shelter in order to avoid predators (Lang 1987;

Webb and Manolis 1989). In contrast, adults as ‘apex predators’ have very few

predators other than humans and larger crocodiles, and as a result are generally not

restricted to sheltered habitat or nocturnal feeding (Lang 1987; Webb and Manolis

1989). Adults are more solitary with individuals coming together only during the

21

breeding season or because drought has restricted the amount of water available

(Webb and Manolis 1989).

Therefore, results from studies that have examined sub-adult and adult C. porosus are

not necessarily applicable to hatchlings. As the majority of studies involving C.

porosus have focused on larger size classes, there is limited information on hatchling

C. porosus. Because growth of hatchling C. porosus within the first year is rapid

(double in size), this will result in changes to their requirements both in the wild and

in captivity. Thus, what is ideal for a new hatchling may not be so for an animal that

is two months, six months, or 12 months of age.

Many of the studies involving hatchling C. porosus in captivity have been

compromised by inadequate temperature control, clutch affects, use of individuals of

different ages and sizes, poor husbandry, and a superficial approach (Garnett and

Murray 1986; Webb et al. 1992; Riese 1991; Mayer 1998; Davis 2001). Subsequently,

results have often been inconclusive or conflicting. This is why there is still no

standard way of raising C. porosus hatchlings (Riese 1991; Davis 2001). A variety of

different methods (pen types, feeding etc) are now being used to raise hatchling C.

porosus, with most farms experimenting with new approaches (Mayer 1998; Davis

2001). However, many of these new practices are often based on assumptions or

anecdotal beliefs not proven by science (Riese 1991; Davis 2001). As the industry has

developed, so to has the commercial confidentiality associated with in-house research,

especially with regard to raising hatchlings (Webb pers. com.). The prevalence of FTT

among captive raised hatchling C. porosus highlights our relative lack of knowledge

22

regarding the requirements of the species at this early developmental stage.

The few studies on wild hatchling C. porosus in Australia occurred in the years

following protection (1977-1991) when the population of C. porosus in Australia was

in a state of recovery (Webb et al. 2000; Letnic 2004). These studies were limited by

low numbers of hatchlings available due to past hunting. In the Northern Territory, the

population is now considered to be approaching pre-exploitation levels, with the

overall size structure now biased towards larger animals which has occurred despite

high levels of egg harvest (Webb et al. 2000; Letnic 2004). The overall change in the

population dynamics, with a shift towards larger individuals, is likely to result in

changes at the hatchling level in terms of growth and survival.

Intended aims and goals of this thesis

It is clear that the hatchling life stage is an important but little understood one, in both

wild and captive conditions. There is a broad range of interrelated factors that are

known or suspected to influence hatchling potential and ultimately fitness, particularly

survival rates, for example egg and thus hatchling size, incubation environment,

absence or presence of parental care, thermoregulation, predation, diet, social

behaviour, movement and dispersal, growth, size-related changes, density, habitat

contexts and more. The degree of importance and overlap of such factors between

wild and captive environments is sometimes obvious (eg. predation), but at other

times obscure (eg. behaviour). A series of these factors is investigated in this study,

the main focus being the poorly understood role of hatchling behaviours. This

23

research provides new information that, combined with existing knowledge, provides

importance guidance about the factors known or likely to affect the survival rates of

hatchling C. porosus. In this study these results were used to guide the design of

experiments aimed at improving growth and survival of this species in captivity and

reducing FTT.

Specific questions addressed through research are:

What are the thermal requirements of hatchling C. porosus, and how are these

influenced by feeding, group size and density, time of day, change in weather

or season, age and size?

What is the nature of agonistic interactions between hatchling C. porosus, how

early do they start and how do they change with age and size, time of day,

feeding, group size and density, distribution of resources, clutch?

Does the nature of agonistic interactions differ between species during this

early life stage?

Can the raising environment be modified based on this information in order to

improve rates of growth and survival of hatchling C. porosus in captivity.

The results of this research will improve our understanding of the thermal and social

requirements of hatchling C. porosus in captivity, and will have broader application to

24

reintroduction and head starting programs involving C. porosus in other countries

where the species is considered threatened or endangered. This study will also provide

the farming industry with information that may improve raising conditions and reduce

the level of mortality.

The thesis is set out as follows. In Chapter 2 the relationship between early growth

and survival of hatchling C. porosus in captivity is examined, Chapter 3.1-3.3 details

the nature of agonistic behaviour and Chapter 4 the nature of thermal behaviour in

hatchling C. porosus. Chapter 5.1-5.4 examines factors affecting growth and survival

of hatchling C. porous in captivity with a focus on agonistic and thermal behaviour,

and Chapter 6 provides a summary, examines the raising environment itself and then

provides conclusions.

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39

Chapter 2. The relationship between early growth and survival of

hatchling saltwater crocodiles (Crocodylus porosus) in captivity

Published as: ‘Brien, M.L., Webb, G.J., McGuinness, K.A., Christian, K.A., 2014.

The relationship between early growth and survival of hatchling saltwater crocodiles

(Crocodylus porosus) in captivity. PloS ONE 9: e100276.

doi:10.1371/journal.pone.0100276’. Formatted according to author guidelines for

journal.

Abstract

Hatchling fitness in crocodilians is affected by ‘runtism’ or failure to thrive syndrome

(FTT) in captivity. In this study, 300 hatchling C. porosus, artificially incubated at

32oC

for most of their embryonic development, were raised in semi-controlled

conditions, with growth criteria derived for the early detection of FTT (within 24

days). Body mass, four days after hatching (BM4d), was correlated with egg size and

was highly clutch specific, while snout-vent length (SVL4d) was much more variable

within and between clutches. Growth trajectories within the first 24 days continued to

90 days and could be used to predict FTT affliction up to 300 days, highlighting the

importance of early growth. Growth and survival of hatchling C. porosus in captivity

was not influenced by initial size (BM4d), with a slight tendency for smaller hatchlings

to grow faster in the immediate post-hatching period. Strong clutch effects (12

clutches) on affliction with FTT were apparent, but could not be explained by

measured clutch variables or other factors. Among individuals not afflicted by FTT (N

= 245), mean growth was highly clutch specific, and the variation could be explained

by an interaction between clutch and season. The results of this study highlight the

40

importance of early growth in hatchling C. porosus, which has implications for the

captive management of this species.

Introduction

Initial offspring size in the wild and in captivity can be expected to confer short to

long term fitness advantages if it improves the ability to forage or capture food, avoid

predation, compete with conspecifics, survive adverse environmental conditions [1]

[2] [3] [4] [5] and ultimately produce more offspring [6] [5]. This has been

demonstrated in a wide range of mammals [7] [8], birds [9] [10], reptiles [11] [12],

amphibians [13] [14], fish [15] [16], and arthropods [17] [18] [4].

Large variation in offspring size and early growth rates are common within and

between species [2] [5], between different populations of the same species [14] [19]

[3], and between siblings from the same clutch [5]. Maternal size and condition [20]

[21] genetic effects [22], multiple paternity, and conditions experienced prior to and

after birth or hatching [22] may all be involved. With several species of mammals

[23], snakes [22], fish [24], and frogs [25], the early nutritional environment is

reportedly just as important as genetic influences in creating irreversible changes in

growth rate and survival which affect long-term fitness [26] [27] [28] [22].

Despite larger offspring size often being correlated with higher rates of initial growth

and survival (‘bigger is better’) [1] [16] [3] [22] [29], there are many exceptions.

There can be small or no effects of initial size on fitness [30] [2] [31], skewed effects

41

in which intermediate sized individuals are the most fit [32], or negative effects in

which initial high growth rates are detrimental to fitness [33] [34]. Among reptiles,

the ‘bigger is better’ hypothesis appears to be generally supported [1] [35] [12] [22],

but there are few data available for crocodilians in the wild or in captivity.

This study examines growth and survival in captive raised hatchling saltwater

crocodiles (Crocodylus porosus), mostly from wild collected eggs (10 of 12 clutches).

Average clutch size for C. porosus in Australia is around 50 eggs (range 2-78; 65.4 to

147.0 g eggs) producing hatchlings from 41.4 to 93.6 g [36] [37]. In the wild an

estimated 54% of hatchlings survive to 1-year-of-age [36] [38], whereas in captivity

survival rates are higher, but vary greatly between establishments using different

raising techniques [39]. The primary cause of mortality in captivity (49% of all

hatchling deaths in captivity) is ‘runtism’ [40] [41] [39] [42], which is in essence a

failure to thrive syndrome (FTT) involving voluntary starvation, which reduces

immunity to disease and causes death between 70 and 200 days post-hatching [40]

[41] [39], with time to death dependent upon initial weight [43]. The root causes of

FTT in hatchlings remain poorly understood, but genetic [39] and incubation effects

[37], elevated corticosterone levels [44], agonistic social interactions [45], and various

aspects of the raising environment (temperature, noise, visual stimuli) and

management protocols (density, size disparity, disturbance) have all been implicated

[46] [40] [41] [39].

Central aims of the present study were to determine the degree to which growth

trajectories established within the first three weeks post-hatching could be used as

42

indices of short-term fitness.. The degree to which size and body condition at hatching

influences post-hatching growth is examined. Particular attention is focussed on

clutch effects on both growth rates and the incidence of FTT. The FTT phenomenon

in C. porosus and its implications on short-term fitness in captivity and in the wild are

discussed.

Materials and Methods

This project was conducted under the approval of the Animal Ethics Committee of

Charles Darwin University (permit no. A11003).

Clutches, eggs and incubation

Saltwater crocodile eggs and hatchlings used in these experiments were provided by

Wildlife Management International (WMI; Darwin, Australia). There were effectively

two groups of hatchlings, those clutches that hatched early in the year (16 - 24

January; 5 clutches; N = 120) when ambient conditions were warmer, and those that

hatched later in the year (Late: 29 March-22 May 2011; 7 clutches; N = 180) when

conditions were cooler. Eggs came from wild nests (N = 10) collected 1 - 50 days

after laying and captive nests (N = 2), collected 1 - 2 days after laying. Egg

temperature within the nest (Tnest) was measured at the time of collection with

calibrated thermometers, 2 - 3 eggs deep in the clutch. Daily fluctuations in Tnest are

reasonably modest but peak at 19:00h to 21:00h [47]. Measured Tnest and the time of

measurement were used as a clutch-specific index for aligning what the mean (Tn.mean)

43

and maximum (Tn.max) nest temperatures may have been up to the time of collection.

Variation in egg size within clutches of C. porosus is low [38], and so mean egg size

(mass, length, width) was measured from only 10 eggs per clutch. All eggs are carried

within the oviducts of females prior to laying, and thus total clutch mass or volume is

the best clutch-specific indicator of female size [38]. The age of each clutch at the

time of collection and the number of infertile eggs and eggs with dead embryos were

estimated using methods described previously [36] [49].

Incubation to hatching (6th

April to 10th

August 2011) was completed for all eggs at

constant 32ºC (± 0.2ºC) and 98-100% humidity, which produces hatchlings with the

highest rates of growth and survival [37]. Eggs were inspected regularly and the

embryos of any dead eggs were used to determine whether death had occurred during

incubation or prior to collection. Hatching typically occurred on the same day for each

clutch. Hatchlings with deformities or which appeared to have excessive abdominal

yolk were excluded from the experiment. Sex was not determined, but 32ºC is a male

producing temperature, and the sensitive period for sex determination for the majority

of eggs (10 of 12 clutches) occurred in the incubator [49] [50] [51]. For the two oldest

clutches, sex may have been determined in the field. One (Tn.mean = 28.6ºC at 50 days)

was probably 100% female, whereas the other (Tn.mean = 33.3ºC at 36 days) may have

contained males and high temperature females [49] [50] [51] [37]. All hatchings were

held in the incubator (32ºC) in crates for three days after hatching before release into

their raising enclosures (day 4) and being fed.

Experimental enclosures

44

Two types of experimental enclosures (initial and final) were used. Hatchlings were

housed between days 4 and 24 in sibling-only groups of 7-10 individuals in the initial

enclosures. They were box shaped (170 x 100 x 50 cm high) fibreglass enclosures

with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x 100

cm; < 8cm deep). At 24 days, hatchlings were transferred into the final enclosures, in

mixed clutch groups of twenty individual hatchlings of similar size. The final

enclosures were 3 m2 box-shaped concrete pens (150 x 200 x 150 cm high), with a

land area (150 x 80 cm) that gradually sloped to a water area (150 x 120 cm; < 19 cm

deep). Each enclosure had a basking cage (100 x 120 cm) attached to the outside and

accessible through an opening (20 x 10 cm) in the wall, which effectively increased

the enclosure area from 3 to 4.2 m2. The cage increased the range of thermal options

available to hatchlings. Hatchlings remained in the final enclosures up until a

maximum of 8 months of age (300 days), but were sorted on the basis of size every 3-

4 weeks [52] [53] [54]. Hence, density remained the same but the individuals in each

final enclosure did not.

A ‘hide area’ [52] [53] [54] was provided in all initial and final enclosures. Each was

80 x 90 cm, constructed of eight lengths (80 cm long) of 10 cm (diameter) PVC pipe

strapped together in the horizontal plane and mounted on legs (5 cm). Hides were

centrally positioned in the water (partly immersed) and overhung the land. One hide

area was provided in the initial fibreglass enclosures, and two in each final enclosure.

All hatchlings were subjected to a natural light cycle. Water temperature (Tw) was

maintained at 31-32°C with thermostatically controlled injection of warm water

45

(initial enclosures) or submerged heating pipes (final enclosures). Air temperature

(Ta) averaged around 32-34°C but varied from 26-36°C at different times of the day

depending on ambient temperatures. All animals were fed chopped red meat

supplemented with di-calcium phosphate (4% by weight) and a multivitamin

supplement (1%) at 16:00-17:00 h six days a week, with waste removed the following

morning (08:00-09:00 h) when the water was changed. Equilibration of Tw after water

changes took 0.5 to 1.5 hours.

Identification and measurements

A uniquely numbered metal webbing tag (Small animal tag 1005-3, National Band

and Tag Co.) was attached to the rear back right foot at the time of hatching. Snout-

vent length (SVL in mm to the anterior of the cloaca) and body mass (BM in grams)

were measured when the animals were introduced into the initial enclosures at 4 days

of age, at 24 days of age when transferred to the final enclosures, and again at 70 to

194 days of age (depending on hatch date). All hatchlings were fasted the day prior to

measurements being taken. Fasting for 48 hours prior to measurement does not affect

growth rates but longer periods of fasting do [43]. These data allowed a size-age curve

to be constructed for each individual, from which, size at 90 days could be predicted,

which avoided problems associated with the different real ages of individuals. These

measurement intervals reflect previous indications that growth patterns established in

the first few weeks and months are an important index of growth and survival after

that time in crocodilians [55]. Hatchling C. porosus that are afflicted by FTT can be

expected to succumb to mortality from 70-200 days post-hatching [39], so although

46

measurements were not taken after 70-194 days, mortalities were recorded up 300

days (10 months) after which survival rates tend to be 95-97% [39].

Statistical analyses

All statistical analyses were performed using JMP 8.0 statistical software [56]. Where

appropriate, data were checked for normality (Shapiro-Wilk’s test) and

homoscedasticity (Cochran’s test) prior to statistical analysis. Morphometric

relationships between egg length (EL) and egg mass (EM) of each clutch with SVL4d

and BM4d; SVL, BM, and body condition (BC = BM /SVL g/mm) at 4 (SVL4d;

BM4d), 24 (SVL24d; BM24d), and 90 (SVL90d; BM90d) days of age, and growth in BM

between 4 and 24 days of age (GBM4-24d) and 24 and 90 days of age (GBM24-90d) were

examined using regression analyses. Size at 90 days was predicted from the size-age

relationship for each individual at 4, 24 and 70 to 194 days (dependent on actual age).

As a check on biases associated with prediction, the actual BM90d and SVL90d of a

sample of animals measured at 90 days (N = 48) were compared with the predicted

values using paired t-tests. No significant difference was detected for the actual and

predicted values of either BM90d (t=0.26; df=94; P=0.79) or SVL90d (t=0.56; df=94;

P=0.58). We examined the effect of season (early: 16-24 January, N = 5; late: 29

March – 22 May, N = 7) on egg mass, hatchling size and growth (SVL and BM) at 4,

24, and 90 days, and %FTT using a PERMANOVA with clutch as a random factor

nested within season. In PERMANOVA, probabilities that treatments are significantly

different from each other are generated by permutation, which requires only limited

assumptions about the distribution of the data: in particular, normality of the data is

47

neither assumed nor required [57]. The analysis was conducted with 1000

permutations in the PERMANOVA+ add-in for PRIMER [57]. Regression analyses

were also used to predict the probability of %FTT affliction up to 300 days from

GBM4-24d and BC24d, and BM24d, using progress means (N = 20 animals). Unequal t-

tests were used to examine differences in BM4d between hatchlings that became

afflicted with FTT (N = 55) and those that survived (N = 245). A Pearson’s chi-square

test was used to examine the effect of clutch on the proportion of individuals that died

from FTT affliction. The effect of clutch on size and growth of non FTT animals (N =

245) was analysed with an ANOVA. All means are reported ± one standard error with

sample sizes.

Results

Clutch, incubation and hatchling characteristics

The wild and captive laid clutches had different numbers of different sized eggs,

which produced different sized hatchlings, came from different sized and aged

females (indicated by total clutch mass). Clutches were collected at different embryo

ages from nests with different temperatures that were laid at different times. Clutches

also had different rates of infertility and embryo mortality before and during

incubation, ultimately producing different proportions of apparently normal hatchlings

(Table 1). The raising experiments also occurred at different times of year, and despite

Tw being constant, Ta varied with the prevailing ambient temperatures.

48

Table 1. Clutch-specific details associated with the hatchlings used in the raising trials and their incubation. ‘30°C days’ is the age an

embryo would be had it been incubated at 30°C [47] [48] [49]. Spot nest temperature (Tn) was measured at the time of collection whereas mean

(Tn.mean) and maximum (Tn.max) nest temperatures are crude estimates [49] [50] [51]. Lay and hatch days: January 1 = day 1. Hatchling sizes were

measured 4 days after hatching, before feeding started. The mean seasonal maximum (Tmax: 13:00h) and minimum (Tmin: 09:00h) air

temperatures during the 21 days of raising for the hatchlings from each clutch (Australian Bureau of Meteorology: Darwin airport). A = wild

nests from the Adelaide River mainstream; BP/CB = captive bred; M = wild nest from Melacca swamp on Adelaide River floodplain.

Clutch ID

Characteristic A20 A44 A70 A71 A75 A77 BP4 CB5 M28 M43 M55 M62

Grand

means

±SD

Age at collection 1 4 24 12 1 1 0 0 16 24 46 42 12.9±15.6

Lay day of year 10 82 125 132 141 141 22 22 15 6 91 114 75.1±56.0

Actual Tn (oC) 29.8 29.8 27.2 28.4 31.9 27.2 30.7 29.5 32.4 32.9 33.2 28 30.1±2.2

Tn.mean (oC) 29.9 31 28.2 29.2 32.2 27.5 31.5 31.4 32.7 33 33.3 28.6 30.7±2.0

Tn.max (oC) 31.8 28.8 31.1 31.4 32.1 32.1 31.8 31.8 31.8 31.8 31.1 31.2 31.4±0.9

Hatch day of year 90 163 198 210 221 221 103 103 98 90 178 182 154.8±51.7

Clutch size (N) 57 45 50 70 50 63 38 47 58 53 53 72 54.7±10.0

Clutch mass (kg) 6.61 4.64 4.52 7.6 5.58 7.21 4.45 5.65 6.7 6.12 6.06 8.09 6.1±1.2

Mean egg mass

(g) 115.9 103.2 90.3 108.6 111.5 114.4 117.2 120.2 115.5 115.5 114.4 112.4 111.6±8.0

Mean egg length

(mm) 78.3 76.8 71.5 79.3 78.8 78.9 80.6 82.4 80.8 81.4 77.9 75.8 78.5±2.9

Mean egg width

(mm) 50.3 48.3 47.1 48.5 50.2 50.2 50.2 49.6 50.2 49.9 50.7 48.9 49.5±1.1

49

Infertile (N) 0 2 2 5 2 4 1 9 14 15 0 0 4.5±5.3

Dead before

collection (N) 1 16 27 17 7 0 0 0 2 0 0 0 5.8±9.1

Dead during

incubation (N) 3 3 0 4 4 4 7 10 4 3 4 1 3.9±2.6

Total dead before

hatching (N) 4 19 27 21 11 4 7 10 6 3 4 1 9.8±8.3

Live remaining

(LR) eggs (N) 53 24 21 44 37 55 30 28 38 35 49 71 40.4±14.6

Abnormal

hatchlings (N) 0 0 0 0 0 0 0 0 0 0 0 1 0.10±0.3

Abundant yolk

hatchlings (N) 0 0 0 1 3 2 0 0 0 0 0 0 0.50±1.0

External yolk

hatchlings (N) 4 1 2 1 5 0 0 4 4 4 0 0 2.1±2.0

Normal

hatchlings (NH) 49 23 19 42 29 53 30 24 34 31 49 70 37.8±15.1

No. NH used in

study 39 19 15 30 15 37 20 17 25 19 25 39 (25.0±9.2)

NH of LR eggs

(%) 92.5 95.8 90.5 95.5 78.4 96.4 100 85.7 89.5 88.6 100 98.6 92.6±6.5

Seasonal Tmin

(ºC)

23.6 17.1 18.7 18.6 19.8 19.8 21.8 21.8 22.7 23.6 19.7 19.3 20.5±0.61

Seasonal Tmax

(ºC) 31.8 28.8 31.1 31.4 32.1 32.1 31.8 31.8 31.8 31.8 31.1 31.2 31.4±0.26

50

Size

Mean EM was highly clutch specific (Table 1), which in turn affected BM4d which is

comprised of hatchling tissue plus the internalised residual yolk mass. Overall, there

was a strong positive linear relationship between mean EM and EL of each clutch and

BM4d but not with SVL4d (Table 2). However, mean clutch EM differed significantly

between seasons (Table 2), with clutches of larger eggs laid earlier in the year (EM

early = 116.86 ± 3.05 g; late = 107.83 ± 2.58 g).

51

Table 2. Relationships between egg length, egg mass, size and growth at 4, 24 and

90 days of age, and % afflicted by Failure to thrive syndrome.

To predict From Formulae

Size and

Growth

BM4d EM

BM4d = 11.677 + 0.541EM + 2.05g; R2 = 0.83; F = 48.74;

P<0.0001

EL

BM4d = -41.856 + 1.445EL + 2.25g; R2 = 0.79; F = 38.78;

P<0.0001

SVL4d EM R2 = 0.10; F = 1.13; P = 0.310

EL R2 = 0.07; F = 0.78; P = 0.400

SVL4d

BM4d

(<70g) R2 = 0.003; F = 0.242; P = 0.620

BM4d

(>70g)

SVL4d = 76.775 + 0.915BM4d + 2.85 mm; R2 = 0.44; F =

164.28; P<0.0001

SVL24d BM24d

SVL24d = -85.632 + 1.290BM24d – (0.00497BM24d)2 ± 4.13 mm;

R2 = 0.60; F = 449.5; P<0.0001

SVL90d BM90d

SVL90d = 147.611 + 0.240BM90d ± 8.82 mm; R2 = 0.94; F =

3865.0; P<0.0001

BM24d BM4d R2 = 0.01; F = 3.14; P = 0.081

BM90d BM4d R2 = 0.01; F = 2.16; P = 0.143

BM90d BM24d

BM90d = -214.090 + 4.179BM24d - 0.0252(BM24d-89.34)2 +

48.69g; R2 = 0.62; F = 241.11; P<0.0001

SVL90d SVL24d

SVL90d = -144.76 + 2.057SVL24d ± 16.29 mm; R2 = 0.44; F =

234.41; P<0.0001

GBM24-90d BM4d R2 = 0.01; F = 2.03; P = 0.161

GBM4-24d BM4d

GBM4-24d = 65.470 - 0.669BM4d ± 15.70 g; R2 = 0.04; F = 12.81;

P = 0.0004

GBM24-90d GBM4-24d

GBM24-90d = 19.146 + 3.147GBM4-24d - 0.0377(GBM4-24d -17.21) ±

50.57g; R2 = 0.44; F = 114.38; P<0.0001

FTT

affliction

%FTT GBM4-24d %FTT = 63.9 - 7.79 GBM4-24d + 10.52; R2 = 0.94; P = 0.0013

BC24d %FTT = 411.8 - 759.12 BC24d + 8.06; R2 = 0.93; P<0.0001

BM24d %FTT = 446.4 - 5.35 BM24d + 6.86; R2 = 0.96; P = 0.0005

Overall mean BM4d of C. porosus (N = 300) was 72.1 ± 4.9 g (55.4-80.8 g), SVL4d

was 144.5 ± 3.8 mm (135-153 mm), and BC4d was 0.50 ± 0.03 g/mm (0.39-0.50

g/mm). However, clutches of eggs laid early in the year produced hatchlings with

52

significantly larger BM4d (75.09 ± 0.38 g) than those produced later in the year (70.15

± 0.31 g; Table 3). However, this was not the case with SVL at 4 days. To examine

the relationship between SVL4d and BM4d the data set was subdivided into <70g (N =

86) and >70g (N = 214) BM4d. There was no relationship between SVL4d and BM4d

for hatchlings with a BM4d <70g, while for hatchlings with BM4d <70g the

relationship was linear (Table 2; Fig. 1a).

Figure 1. Relationship between BM and SVL of hatchling C. porosus (N = 300) at

different ages. Relationship at a) 4d, b) 24d, and c) 90d for hatchlings born early (N

= 120; blue) and late (N = 180; grey) in the year. BM90d was predicted from the size-

age relationship for each individual at 4, 24 and 70 to 194 days.

At 24 days of age, the overall mean BM24d of C. porosus (N = 300) was 89.3 ± 15.8 g

(60-142 g), SVL24d was 159.6 ± 7.0 mm (143-178 mm), and BC24d was 0.55 ± 0.08

g/mm (0.41-0.80 g/mm). Clutches of hatchlings born later in the season were not

significantly heavier at 24 days than those born early in the year (Table 3). In contrast

to the highly variable relationship between SVL and BM at 4 days, there was a much

stronger relationship between BM and SVL at 24 days (Table 2; Fig. 1b).

53

Based on predictions at 90 days of age (N = 300), mean BM90d was 162.7 ± 75.9 g

(37-409 g), SVL90d was 187.7 ± 24.8 mm (147-250 mm), and BC90d was 0.80 ± 0.33

mm (range 0.25 to 1.62 g/mm). There were no significant seasonal differences in

SVL90d or BM90d (Table 3). The relationship between SVL and BM at 90 days of age

was strongly linear (Table 2; Fig. 1c).

Growth

Given the relatively uniform size of hatchling BM at 4 days (SD of BM4d = ±4.9 g)

the individual variation in size by 24 days (SD of BM24d = ± 15.8 g) and 90 days (SD

of BM90d = ± 78.6 g) was extreme and was reflected in BC. Mean GBM4-24d was 17.2 ±

16.0 g but the range (-6.9 to 70.1 g) was already extreme with some individuals

increasing by 70 g (+97.5%BM4d) while others had lost 7 g (-9.3%BM4d). Mean

GSVL4-24d was 15.4 ± 6.9 mm (range 1 to 30 mm). Mean GBM24-90d (63.7 ± 67.1 g;

range -40.2-278.6 g) and GSVL24-90d (24.2 ± 17.91 mm; range -3 to 77) both increased

substantially relative to the 4-24 day period, but variation remained extreme. There

were no seasonal differences in SVL or BM growth (Table 3).

54

Table 3. Seasonal differences in size, growth and %FTT between clutches laid

early in the year (16-24 January 2011; 5 clutches) and clutches laid late in the

year (29 March-22 May 2011; 7 clutches) using PERMANOVA with d.f. as 1 and

10.06.

Early vs late clutches Pseudo-F P(Perm)

EM 5.11 0.04

BM4d 8.09 0.02

SVL4d 1.70 0.23

BM24d 0.01 0.76

SVL24d 4.64 0.06

BM90d 0.79 0.43

SVL90d 1.06 0.33

GSVL4-24d 1.30 0.27

GBM4-24d 2.50 0.14

GSVL24-90d 0.11 0.77

GBM24-90d 1.25 0.33

%FTT 1.71 0.22

There was no significant relationship between BM4d and either BM24d, BM90d, or

GBM24-90d (Table 2). However, BM4d did have a slightly significant but highly variable

relationship with GBM4-24d (Table 2), with higher growth among the smallest

hatchlings born. Growth trajectories in BM and SVL established within the first 24

days were largely continued up to 90 days (Fig. 2; Table 2). A high proportion of

individuals with the lowest GBM4-24d and GSVL4-24d and smallest BM24d and SVL24d

failed to recover by 90 days (Fig. 2).

55

Figure 2. Relationship between size and growth of hatchling C. porosus (N = 300)

at different ages. Relationship at 24 and 90 days: a) BM24d and BM90d, b) SVL24d and

SVL90d, c) GBM4-24d and GBM24-90d, and d) GSVL4-24d and GSVL24-90d for hatchlings born

early (N = 120; blue) and late (N = 180; grey) in the year.

Survival - FTT affliction

All animals which died during and after the study (<300 days post-hatching) were

recorded. Of these, 55 (72% of mortalities) were seriously afflicted by FTT, did not

respond to efforts to stimulate feeding, and died or were euthanized [31 (56.4%) at

70-100 days 15 (27.3%) at 100-130 days; 9 (16.4%) at 130-202 days]. The remainder

included animals (N = 17) that were otherwise healthy that died for other reasons

between 90 and 300 days post-hatching. The proportion of individuals that died from

FTT was not significantly different between seasons (Table 2).

56

BM4d was not significantly different between those hatchling afflicted by FTT (N =

55) and those that survived (N = 245; unequal t-test: t=-0.429; df=298; P=0.668).

However, the probability of affliction with FTT was clearly indicated within the first

24 days, by the extent of growth in body mass (Table 2; Fig. 3a), body condition

(Table 2; Fig. 3b), and body mass (Table 2; Fig. 3c). No affliction by FTT (0%FTT)

was detected in animals that grew more than 8.2 g, achieved a BC24d of 0.55 g/mm

SVL or a BM24d of 81.7 g in the first 24 days post-hatching. However, there were a

total of 55 hatchlings that grew less than 8.2 g after 24 days and survived. These

hatchlings grew significantly less (44.43 ± 4.59g; Welch’s t-test: t = 7.49; df = 243;

P<0.0001) between 24 and 90 days and were significantly smaller at 90 days (122.48

± 4.67g; Welch’s t-test: t = 9.82; df = 243; P<0.0001) compared with other hatchlings

(GBM24-90d= 92.03 ± 4.40; BM90d= 189.28 ± 4.95).

57

Figure 3. Probability of avoiding FTT and surviving to 300 days for hatchling C. porosus (N = 300) in relation to a) GBM4-24d, b) BC24d,

and c) BM24d. Points are means for progress intervals (N = 20).

58

Clutch effects

Among the non-FTT individuals (N = 245), clutch had a significant effect on BM4d,

GBM4-24d, and BM24d (Table 4). As growth trajectories established within the first 24

days are continued to 90 days, clutch effects were also apparent in GBM24-and BM90d

(Table 4). However, if the variance due to GBM4-24d is removed, no remaining clutch

variation occurred in BM24d, GBM24-90d, or BM90d. This confirms that the clutch

variation detected was mainly due to variation in GBM4-24d.

59

Table 4. BM4d, BM24d, BM90d, GBM4-24d, GBM24-90d, and for non-FTT animals (N = 245) and the percentage of FTT animals (N=55)

according to clutch.

Variable ANOVA Clutch ID

A20 A44 A70 A71 A75 A77 BP4 CB5 M28 M43 M55 M62

BM4d (g) R2=0.68; F=45.14; P<0.0001

Mean 73.9 67.6 61 72.2 71.6 71.9 77.3 77.7 74.5 73.9 76.2 67.8

SD 3.3 1.9 3.4 2.2 3.7 3.6 1.8 2.4 2.7 2.2 2.6 3.1

BM24d (g) R2=0.24; F=6.62; P<0.0001

Mean 85.6 99.2 82.6 101.6 88.6 102.4 92.9 98.7 84.8 83.2 92.6 97.3

SD 7.1 16.2 10.5 17.1 3.7 18.9 13.1 12.6 10.9 5.5 8.5 13.5

BM90d (g) R2=0.23; F=6.23; P<0.0001

Mean 142.2 181.1 125.3 185.6 123.1 215.3 158.6 260.9 152.6 111.5 96.9 178.8

SD 56.9 73.3 70.9 64.5 18.6 86.0 88.4 61.4 60.8 53.2 54.2 53.0

60

GBM4-24d

(g) R2=0.32; F=10.01; P<0.0001

Mean 11.7 31.6 21.6 29.4 16.9 30.5 15.6 20.9 10.3 9.3 16.4 29.5

SD 6.3 15.9 9.3 16.9 4.1 18.4 12.3 12.4 9.6 5.3 9 13.2

GBM24-90d

(g) R2=0.23; F=6.23; P<0.0001

Mean 68.0 81.9 58.9 82.1 34.5 112.9 83.7 162.3 72.5 52.7 42.9 84.3

SD 43.8 61.9 62.8 59.1 18.6 74.5 68.7 50.5 49.6 34.7 42.3 41.7

%FTT 10.3 0 20 23.3 53.3 27 15 0 8 26.3 48 2.6

61

Across clutches, the mean incidence of FTT was 19.5 + 4.99% of hatchlings, but the

range varied from 0% to 53.3%, demonstrating highly significant clutch effects (X2 =

48.36, df = 11, P < 0.0001; Table 4). None of the clutch-specific variation in %FTT

could be explained by the mean clutch and incubation characteristics (Table 1),

although it was a relatively small sample (N = 12) and none of these variables were

controlled.

Discussion

Our results suggest that under similar experimental conditions, growth trajectories for

the majority of C. porosus hatchlings established within the first 24 days post-

hatching extend to 90 days and beyond. Similarly, individuals with a high probability

of affliction by FTT up to 300 days post-hatching can be identified within the first 24

days by reduced growth. Therefore, instead of conforming to the ‘bigger is better’

hypothesis, hatchling C. porosus under these conditions appear to benefit from rapid

early growth. However, whether this is the situation in the wild, where the

environment is vastly different to that in captivity, is unknown.

While insights into the fitness of animals can be gained from both captive and wild

animals, results need to be merged and assessed carefully. Growth and survival of

neonate snakes (Thamnophis sirtalis) under captive conditions were similar to those in

the field [12] [58]. Yet other animals held in captivity can experience either greater or

less fitness than their wild counterparts. Species which suffer high levels of stress [59]

in captivity generally appear to be less fit, and this has been reported in certain species

62

of lemur [60] [61], dolphin [62] [63], parrot [64] [65], and raptor [66], and predictably

so if their ecology and response to humans is considered [67] [59].

For hatchling C. porosus under captive conditions, resources such as temperature,

cover and food are abundant and there is no risk of predation [55]. However,

individuals are confined and forced to live at higher than natural densities, and are

subject to human disturbance [55]. In the wild, the availability of resources can often

be limited or can fluctuate while the threat of predation is high and hatchling C.

porosus must contend with larger crocodiles [36] [49]. Female C. porosus also protect

their offspring for the first few weeks and months post hatching [36] [49]. As such,

differences may exist in terms of which traits (size etc) may be selected for in

captivity and in the wild, and this in turn may vary according to location and habitat.

For C. porosus, and many other crocodilians, there may be advantages in attaining a

large size rapidly, in terms of the ability to avoid predation, compete with

conspecifics, survive adverse environmental conditions, and reach sexual maturity

[68]. In the majority of cases, aggressive encounters between crocodilians favour the

larger animal [45] [69] [70], which then enables greater access to resources and

subsequently improved long-term fitness both in the wild and in captivity [68] [55].

Crocodylus porosus is considered the most aggressive and intolerant of conspecifics

of all crocodilians [70], and agonistic behaviour begins within two days of hatching

[45]. Such behaviours are known to affect growth and survival in several species of

reptile [71] [72] [73] [74], and this also appears to be the case in C. porosus under

captive conditions [55] [75] [39].

63

Clutch of origin and the incubation environment have been widely reported to affect

post-hatching growth and survival in crocodilians [42] [76] [77] [37] [78] [39].

Therefore, we tried to quantify sources of variation within the clutch, egg and

incubation variables that may have biased our results (Table 1). None explained the

variation in growth or affliction with FTT. However, the results highlight the inherent

complexity of potential variables that may influence growth and survival, and the

importance of assumptions about the homogeneity of neonates used for such raising

trials [42] [39].

That FTT can be predicted after 24 days, suggests that the first few weeks post-

hatching are crucial to short-term fitness of C. porosus under captive conditions with

survival increasing up to 90% in individuals that increased in mass by 4-7g during this

period. While this has been suggested for crocodilians by previous authors [37] [55],

it has never been accurately quantified for any species. Regardless of whether this is

the situation in the wild it does suggest that if early conditions are unfavourable,

short-term growth and survival can be compromised. This has been found in water

pythons [22] in which different rates of growth and survival occur between years

based on prey abundance during the early post-hatching stage.

The occurrence of FTT among captive-raised crocodilians is widespread, although

because weakened animals are vulnerable to secondary illnesses, FTT may be under-

reported [41]. Regardless, C. porosus appear particularly prone to FTT affliction [40]

[42] [39]. FTT is generally considered to result from an inadequate raising

64

environment, but what constitutes an adequate raising environment for each species

remains poorly understood and may be more species-specific than previously realised.

For example, Alligator mississippiensis have substantially higher rates of growth and

survival to one year of age when raised under identical conditions to C. porosus [82]

[73]. Hatchling A. mississippiensis are reported to initiate feeding more rapidly and on

a wider range of food types, and as a species are considered far more tolerant of

conspecifics with no or little aggression reported among juveniles in captivity [79]

[68] [55] [70]. Therefore, it is possible that the current approach to raising C. porosus

in captivity, which was originally based on the model used for A. mississippiensis [79]

[68], may be inadequate.

The extent to which FTT occurs in wild populations of C. porosus is not well

understood, and would be difficult to quantify due to (presumably) an increased

vulnerability of these weakened animals to predation. However, while emaciated or

malnourished hatchling C. acutus [80], A. mississippiensis, and C. johnstoni (M.

Brien pers. observation) have been observed in the wild on a number of occasions,

hatchling C. porosus in an emaciated state have rarely been encountered in the wild

[81] [82]. Hence FTT may not occur in wild C. porosus at anything like the rates

reported in captivity [39]. If so, genetic predispositions to FTT, which could be

complicated by multiple paternity [83], may be a response to threats that can be

avoided by appropriate behaviour in the wild, but not in captivity.

Factors that affect survival rates in hatchling C. porosus under captive conditions have

clear implications on future growth and survival. However, it is not really clear that

65

enhanced growth trajectories in the hatchling stage, forewarned in the first 24 days,

will ultimately influence ‘fitness’ of individuals in the long-term. It is unlikely that

measured variation in growth within a time scale of 24 days will ultimately be

correlated with variation in reproductive performance after a time scale of up to 20+

years depending on species [38] [84]. This is because a completely different suite of

factors dictate progress and outcomes during this time [85].

Variation in the survival and growth rates of C. porosus hatchlings in controlled

environments are intimately connected to each other, particularly through FTT.

Absolute growth, independent of hatchling size, is perhaps the best index of

individual performance, which has implications for survival within captive

environments, where the goal is often to enhance both survival and the early

attainment of large juvenile size. However, it is important to realise that some

hatchlings can recover from poor growth rates within the first 24 days (<8.2 g).

Identifying and understanding the causes of FTT among hatchling crocodilians is

essential for improving conservation and management programs aimed at raising

crocodilians that are threatened or endangered for purposes such as head starting, in

which individuals are released back to the wild at a size that ensures greater survival.

Acknowledgements

We thank Jemeema Brien and Charlie Manolis for their help in different phases of the

project. We would also like to thank Wildlife Management International for the

supply of animals, use of facilities, logistical support and major funding for this

66

project. WMI funding through the Rural Industries Research and Development

Corporation is gratefully acknowledged. Funding was provided through a Holsworth

Wildlife Research Endowment (ANZ Trustees Foundation), Northern Territory

Research and Innovation Board student grant, and Charles Darwin University.

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Chapter 3.1. Born to be bad: agonistic behaviour in hatchling

saltwater crocodiles (Crocodylus porosus)

Published as: ‘Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian,

K.A., 2013. Born to be bad: agonistic behaviour in hatchling saltwater crocodiles

(Crocodylus porosus). Behaviour 150: 737–762’. Formatted according to author

guidelines for journal.

Summary

Detailed observations on groups of captive saltwater crocodile (Crocodylus porosus)

hatchlings revealed sporadic periods of intense agonistic interactions, with 16 highly

distinctive behaviours, in the morning (0600-0800 h) and evening (1700-2000 h) in

shallow water. Ontogenetic changes in agonistic behaviour were quantified by

examining 18 different groups of hatchlings, six groups each at 1-week, 13-weeks,

and 40 weeks after hatching. Agonistic interactions between hatchlings at 1 week of

age (mean: 7.3 ± 0.65/night) were not well-defined and varied in intensity (low,

medium, high), number of individuals that were aggressive, and the outcome, while

most interactions involved contact (94.5%). There were also clutch specific

differences in the frequency of agonistic interactions. At 13 and 40 weeks, a more

hierarchal dominance relationship appeared to be established which primarily

involved aggression-submission interactions. Agonistic interactions were more

frequent (13 weeks: 9.7 ± 0.61/night; 40 weeks: 22.2 ± 0.61/night) and intense

(medium, high), but shorter in duration, in which the subordinate individual fled in

response to an approach by a dominant animal that often gave chase but did not make

80

contact. While the full repertoire of behaviour was displayed by hatchlings at 1 week

of age, a smaller subset based on dominance status was displayed among 13 and 40

week old hatchlings. Agonistic behaviour occurs in C. porosus shortly after hatching

and is important in establishing and maintaining dominance hierarchies that are

characterised by aggression-submission interactions. This type of interaction appears

typical for C. porosus both in the wild and in captivity, and may be important in

preventing serious injury in a species equipped with formidable armoury. Dispersal by

hatchling C. porosus at around 13 weeks of age appears to be driven by a growing

intolerance of conspecifics, while territoriality is apparent at an early age.

Consequently, agonistic behaviour and social status may be major contributors to the

observed differences in growth rates and survival in captivity.

Keywords: agonistic behaviour, Crocodylus porosus, dominance, hatchling crocodiles,

ontogenetic change

Introduction

Agonistic behaviour is defined as any behaviour related to aggression and includes

displays, threats, physical contact, submission, and retreats (Schenkel, 1967; Hinde,

1971; Wilson, 1975). Agonistic behaviour has been widely reported in many taxa,

including birds (Drummond, 2001; Dickinson et al., 2009), fish (Bergman, 1968;

Genner et al., 1999), mammals (Bekoff et al., 1981; Smale et al., 1995), amphibians

(Wells, 1980; Staub, 1993), crustaceans (Huber & Kravitz, 1995), and reptiles

(Stamps, 1977; Phillips et al., 1993), and is known to affect access to resources, which

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in turn influences rates of growth and survival (Drummond, 2006).

Agonistic behaviour is an integral part of establishing and maintaining dominance

hierarchies in a range of taxa that coexist in groups for at least part of their life

(Krause & Ruxton, 2002; Drummond 2006). The establishment of a dominance

hierarchy can often reduce the frequency of actual physical contact, and thus injury

(Carpenter & Ferguson 1977; Lumsden & Holldobler 1983), which can be especially

important among species equipped with dangerous weaponry (Huber & Kravitz,

1995). Therefore, understanding the onset and ontogeny of agonistic behaviour, and

the nature of dominance, is relevant to the species’ ecology in nature and in captivity.

Although social behaviour among newly hatched or born reptiles has seldom been

studied, agonistic behaviour is believed to start early, reach maximum intensity

quickly (Drummond, 2006), and become involved in the early establishment of

dominance hierarchies in some lizards (Phillips et al., 1993; Goetz & Thomas, 1994;

Worner, 2009), snakes (Barker et al., 1979; Carpenter, 1984) and possibly turtles

(Froese & Burghardt, 1974). Agonistic behaviour and social dominance are also

linked to variation in juvenile growth and survival rates in some reptiles (Carpenter &

Ferguson, 1977; Stamps & Tanaka, 1981; Castanet et al., 1988; Phillips et al., 1993;

Goetz & Thomas, 1994; Worner, 2009).

Crocodilians are behaviourally complex reptiles (Garrick & Lang, 1977; Garrick et

al., 1978; Lang, 1987; Vliet, 1989; Thorbjarnarson & Hernandez, 1993), in which

agonistic behaviour is well established and interacts in complex ways with other

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behaviour (e.g. thermoregulation, feeding, movements and habitat use) (Lang, 1987;

Seebacher & Grigg, 2000). However, detailed studies of social behaviour are limited

to adults of only a few of the 23 extant species, most notably the American alligator

(Alligator mississippiensis) (Garrick & Lang, 1977; Garrick et al., 1978; Vliet, 1989),

Nile crocodile (Crocodylus niloticus) (Cott, 1961; Modha, 1967; Pooley, 1969), and

American crocodile (Crocodylus acutus) (Garrick & Lang, 1977; Thorbjarnarson,

1991). Agonistic behaviour has been opportunistically reported among juvenile

Crocodylus johnstoni (Webb et al., 1982), C. niloticus (Morpurgo et al., 1993),

Crocodylus porosus (Messel et al., 1981; Bustard & Maharana, 1983) and A.

mississippiensis (Joanen & McNease, 1987), but has not been documented or

examined thoroughly early in life in any crocodilian species.

Of the extant crocodilians, saltwater crocodiles (C. porosus) are considered the

most aggressive and least tolerant of conspecifics (Lang, 1987). Yet in the immediate

post-hatching period (first few weeks), hatchling C. porosus exist in nest-specific

crèches, that may be joined by hatchlings from other nearby crèches (Webb et al.,

1977). They undertake group activities, such as crossing rivers together, and

hatchlings appear to exhibit high levels of tolerance to each other (Webb et al., 1977).

Agonistic behaviour and social dominance may be responsible for hatchling C.

porosus eventually dispersing from crèches by 2-3 months (8-12 weeks) of age in the

wild (Webb & Messel, 1978). If so, in captive situations, where the ability of

hatchlings to disperse is limited, agonistic behaviour may be implicated in social

structuring within a group, creating the high variability in individual growth rates

reported (Onions, 1987; Webb et al., 1987; Webb & Smith, 1987; Mayer, 1998;

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Isberg et al., 2009). This in turn has been implicated in the 10-40 % of C. porosus

hatchlings that do not survive (Webb et al., 1987; Isberg et al., 2009). By 1-2 years of

age, agonistic behaviour in C. porosus is reportedly well established both in the wild

(Messel et al., 1981) and in captivity (Bustard & Maharana, 1983; Lang, 1987).

However, the situation that exists within the first year of life is largely unknown, with

only one unpublished study (Riese, 1991) reporting agonistic behaviour among

hatchling C. porosus in captivity.

In this study, we examined agonistic behaviour among captive C. porosus at three

important life history stages: 1 week (crèche together), 13 weeks (dispersal occurs),

and 40 weeks (solitary and much larger size) after hatching, with the following

objectives:

a. Determine the extent to which hatchling C. porosus engage in agonistic

interactions from the first week of life onward;

b. Describe and quantify agonistic behaviour that may be used by hatchling C.

porosus to elicit and respond to aggression;

c. Quantify any ontogenetic changes in agonistic interactions (1, 13 and 40 weeks)

in terms of frequency, timing, duration, intensity of interaction and the types of

behaviour used; and,

d. Discuss the implications of agonistic behaviour and dominance in C. porosus

hatchlings in the field and in captivity, and in relation to other taxa.

Materials and methods

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Subjects and Housing

In August-December of 2011, 90 captive-born hatchling saltwater crocodiles

(Crocodylus porosus), in three age cohorts, were provided by Wildlife Management

International (WMI; Darwin, Australia). The first cohort (N = 30) contained

individuals from six different clutches, one week after hatching, while the second (13

weeks after hatching; N = 30) and third (40 weeks after hatching; N = 30) cohorts

contained hatchlings from a further five and seven different clutches respectively, that

were of similar size and age. These age cohorts were based on the early life history of

C. porosus (see Introduction), along with previous observations of behaviour. Using

the same crocodiles throughout the study was initially considered but not feasible, due

to the highly variable nature of growth within and between different clutches for this

species. Because some individuals can be almost 2-3 times the size of others by 1-2

months of age, this can lead to the death of smaller animals. In most cases, using the

same animals would simply not have been possible as 10-40% of hatchling C. porosus

in captivity die during the first 3-8 months of life (despite best practices), and this can

be higher (80-100%) for certain clutches (Webb et al., 1987; Isberg et al., 2009).

All crocodiles originated from eggs collected from wild nests in the Northern

Territory of Australia, between December and February shortly after they were laid

(10-25 days old). These eggs were then artificially incubated at a constant 32ºC and

100% humidity until they hatched (March-May). After hatching, all crocodiles were

held in the incubator for three days to assist the assimilation of residual yolk before

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they were released as sibling only groups into the same type of enclosure (day 4).

Only crocodiles that had experienced similar environmental conditions during

incubation, and were considered ‘normal’ (healthy size and weight, no deformities)

were used in experiments. All hatchlings were subject to the same raising conditions

(enclosure, temperature, and husbandry) prior to, and during the experiments. For the

one week old cohort, 5 individuals from 6 separate clutches that hatched on the same

day (N = 30) were used, whereas the 13 and 40 week hatchlings came from clutches

of different origin, and were placed into the same experimental enclosures, at the

same density (5 per pen) and on the same day.

For each animal, snout-vent length (SVL - mm), total length (TL - mm), and body

mass (g) were measured and a uniquely numbered metal webbing tag (Small animal

tag 1005-3, National Band and Tag Co.) was attached to the rear right foot. Mean size

of 1-week olds (N = 30) was 144.7 ± 0.31 mm (SE) SVL, 308.8 ± 1.2 mm TL, and

71.1 ± 0.43 g mass. Mean size of 13-week olds (N = 30) was 209.0 ± 1.6 mm SVL,

442.4 ± 2.7 mm TL, and 254.5 ± 5.6 g mass, while the mean size of 40 week olds was

345.3 ± 1.6 mm SVL, 704.2 ± 2.5 mm TL, and 836.0 ± 4.28 g. Sex was determined by

manually probing the cloaca. The majority of crocodiles in all age cohorts were male

(3-5 in each group), and this was attributed to the incubation temperature (32ºC)

(Webb et al., 1987).

The fibreglass enclosures used to house all experimental groups were box shaped

(170 × 100 × 50 cm), with a land area (70 × 100 cm) that gradually sloped down to a

water area (100 × 100 cm; < 8cm deep). Therefore, all hatchlings were at a density of

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2.9 animals per m2 which was considered very low based on previous studies (Garnett

and Murray 1986; Riese, 1991; Mayer, 1998). These studies determined that the

optimal density for raising hatchling C. porosus, in terms of growth and survival, was

10-15 animals per m2. A ‘hide area’ (Riese, 1991; Mayer, 1998; Davis, 2001) was

provided in each enclosure, and was constructed with 8 lengths (80cm long) of 10 cm

PVC pipe strapped together and on legs, centrally positioned in the water (partly

immersed) and overhanging the land. Water temperatures were maintained at 30-

32°C, air temperatures varied from 26-32°C, and there was a natural light cycle. All

animals were fed on chopped red meat supplemented with di-calcium phosphate (4%)

and a multivitamin and mineral supplement (1%), which is the standard diet, fed to

hatchling C. porosus in captivity. Enough food for each individual was made

available throughout the night (1600-0900h), which is when hatchling C. porosus are

known to feed in captivity and in the wild (Lang, 1987). Waste removal and cleaning

occurred the following morning (0900 h) when the water was changed.

Recording Behaviour

Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure were used to

record all behaviour on digital video recorders (Signet 4CH DVR QV-8104). The

recording period lasted 15 hours (1700 to 0800 h) and was conducted on 3

consecutive nights for each group (45 hours per group). This daily sampling period

was based on previous recordings (100’s of hours) that revealed no agonistic

behaviour occurring between 0800 and 1700 h, with hatchlings spending the majority

of the day inactive and hiding under cover. The recordings were taken 4-5 days after

87

the crocodiles were placed in the new experimental enclosures. The only exception

were the 1-week groups in which some recordings were taken immediately after

release (when individuals were 4-5 days of age) to determine whether agonistic

behaviour or behaviour patterns were already present, and then again at 6-8 days.

Agonistic Interactions

An agonistic interaction was defined as any interaction between individuals in which

aggression and intolerance was signalled by postures or actions by one or both

individuals. An aggressive individual was one that made aggressive advances toward

another and/or made physical contact with another. Each agonistic interaction was

examined to quantify whether one or both contestants engaged in aggression. The

intensity of agonistic interactions was characterised as: low, medium or high. Low

intensity interactions were accidental, occurring when individuals lying together

appeared to disturb each other when moving, or if one swam into another underwater.

Medium and high intensity interactions appeared deliberate, with one individual

approaching another with the goal of initiating an agonistic interaction. High intensity

interactions were distinguished from medium intensity interactions by the display of

more intense contact behaviour. The behaviour exhibited, the intensity of interaction

(low, medium, high), the location (water, hide, land), the time, duration of interaction

and outcome were all quantified from the tapes.

Classification of Behaviour

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Behavioural observations recorded during these experiments were used to create an

inventory of agonistic behaviour for C. porosus hatchlings. The descriptions are based

on a series of basic postures, modified by movement of body parts, or of the whole

animal, and whether visual signals or actual contact was involved. Some of these

behaviours have been described in other studies with adult crocodilians (Garrick &

Lang, 1977; Lang, 1987).

Statistical Analyses

All statistical analyses were performed using JMP 8.0 statistical software (SAS

Institute Inc., 2010). Where appropriate, data were checked for normality (Shapiro-

Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. A

repeated-measures ANOVA was used for comparison of means between 1 week, 13

week, and 40 week old hatchlings, with night of recording (N = 3) as the repeated

measure. A Pearsons’ Chi-square test was used to compare intensity, outcome, contact

made, number of individuals aggressive, and how often the instigator won, where

sample sizes were adequate. To test whether variation in the frequency of interactions

could be explained by time of day, the results were grouped into one of three periods:

dusk 1700-2000 h; night 2000-0600 h; and dawn 0600-0800 h. A significance level of

P<0.05 was used for all statistical tests. All means are reported ± one standard error

with sample sizes.

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Results

All agonistic interactions were in open water with none occurring on the land or near

the food on land. Some interactions were initiated accidentally, when individuals

lying together appeared to disturb each other when moving, or if one swam into

another underwater. All agonistic interactions between hatchling C. porosus involved

only two individuals at any one time. Most interactions were initiated by one or both

individuals moving deliberately toward each other, in a rapid advance (RA),

consisting of a series of short, rapid movements (Table 1). In response to RA, one or

both individuals would adopt a series of other agonistic behaviour. These involved the

adoption of some discrete postures, which often varied in the intensity of expression

(Table 1; Figure 1).

The adoption of such postures could be abandoned at any time by either slow (SF)

or rapid flight (RF), ending the agonistic interaction. Alternatively, the signals

emanating from the postures could be intensified with body movements, such as light

jaw claps (LJC) or tail wagging (TW), which were displays, not involving physical

contact with combatants. If the agonistic interaction was still not terminated by flight

of one or both animals, the behaviour intensified further, with contact movements

such as head pushing (HP), biting (B) or side head striking (SHS), often combined in

different ways with intense tail wagging (Table 1; Figure 1), until one or both

individuals took flight.

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Table 1. Classification of the behaviour used by hatchling C. porosus during

agonistic interactions. Responses to aggression can be graded, involving the adoption

of static postures, followed by non-contact movements followed again by contact

movements.

Abbreviation Definition

Initiation

Rapid advance RA Series of short rapid advance movements towards another

individual while LIW.

Termination

Slow flight SF Slow movement away from another individual in a LIW

posture.

Rapid flight RF Rapid movement away from another individual in a LIW

posture.

Chase C Rapid movement toward another individual in a LIW

posture.

Posture

Low in water LIW Immobile with only the top of the head and back above the

water surface (Figure 1a).

Inflated posture IP* Immobile with upward extension of either the front two or

all four limbs, with neck and back arched high and head and

tail angled downward (Figure 1b).

Head and tail raised HTR* Immobile with head and tail raised out of water while back

remains low. Head is usually parallel to the water but can

also be angled upwards (Figure 1c).

Head raised high

HRH*

Immobile with upward extension of the front two limbs

pushing the head and chest high out of the water on a ~45º

angle while tail remains low (Figure 1d).

Mouth agape MA* Immobile with mouth opened wide (in combination with

postures LIW, IP, HTR or HRH; Figure 1e).

Non-contact

movements

Light jaw-clap LJC* Rapid opening and closing of the jaws at the water surface,

often repeated several times (LIW or IP posture; Figure 1f).

Tail-wagging TW* Undulation of the tail from side to side in either a gentle

sweeping motion or rapid twitching, often repeated several

times (all postures; Figure 1g).

Contact movement

Head push HP Head is pushed in to an opponent, usually with mouth closed

(LIW or IP posture).

Bite B Jaws closed shut on an opponent (all postures).

Side head-strike SHS Head is thrust sideways in to an opponent while the mouth is

either open or closed (all postures).

Tail-wag side head

strike

TWSHS Tail wagging occurs prior to a side head strike, increasing

the force of the impact (all postures; Figure 1h).

Tail-wag bite TWB Tail wagging occurs prior to a bite which propels the

individual in to an opponent with force (LIW posture; Figure

1i).

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*behaviour previously described by Garrick & Lang (1977) and Lang (1987)

Figure 1. Postures, non-contact and contact movements, described in Table 1,

displayed by hatchling C. porosus during agonistic interactions at 1, 13 and 40 weeks

of age.

Ontogenetic Changes

1. Aggression

An aggressive individual was defined as one that made aggressive advances toward

92

another and, or which made physical contact with another animal. Each agonistic

interaction was examined to quantify whether one or both contestants engaged in

aggression, and whether this differed across age classes. The number of interactions in

which both individuals were aggressive was highest at 1 week of age (37.9% of

interactions involved both individuals displaying aggression) and decreased

significantly with age. At 13 and 40 weeks, only 2.3% and 0.0% of interactions

respectively involved both individuals being aggressive. The number of separate

movements or steps in the RA increased significantly with age (F2,15 = 4.63, P <

0.05), from a mean of 1.61 ± 0.18 (mean of means; range 0-7; N = 6) per interaction at

1 week to 3.62 ± 0.11 steps (range 0-12; N = 6) at 40 weeks.

2. Frequency

Filming during the first two nights in the enclosure (hatchlings 4-5 days old)

confirmed agonistic interactions were already occurring. Frequency of agonistic

interactions was determined from film records for days 6-8 in the 1 week old cohort.

In all six groups of 5 hatchlings, the mean number of agonistic interactions per group

per night was 7.3 ± 0.65 (mean of means; N = 6, range 3-13). The frequency of

agonistic interactions was significantly higher among the older age cohorts (F2,15 =

6.75, P < 0.05), with 9.7 ± 0.61 (N = 6, range 6-14) at 13 weeks old, and 22.2 ± 0.61

(N = 6, range 12-34) at 40 weeks old.

3. Timing

93

For all three age cohorts combined, the frequency of agonistic interactions at dusk

(1700-2000 h), night (2000-0600 h) and dawn (0600-0800 h) varied significantly

(F2,14 = 13.46, P < 0.05). The majority of agonistic interactions occurred in the early

evening (1700-2000 h), with about half as many in the early morning (0600-0800 h)

(Figure 2). Agonistic interactions were rare during the night (2000 to 0500 h), when

the 1 week old hatchlings would often lie together in contact, in the water, in groups

of 2-5 individuals. The 13 and 40 week old hatchlings were non-aggressive during the

same period, but were rarely observed lying in contact with each other.

Figure 2. Percentage of agonistic interactions (%) as a function of hour (1700-0800

h) for C. porosus housed in groups of 5 at three different ages (1, 13 and 40 weeks).

4. Postures

The postures displayed in agonistic interactions, as deemed to be aggressive and non-

aggressive, varied across the three age cohorts (Table 2). When both individuals were

94

aggressive, they typically aligned head to head, usually parallel to each other before

assuming a HTR, IP, or HRH posture (Table 1; Figure 1). At one week old, aggressive

hatchlings were more likely to assume a range of postures during an agonistic

interaction than hatchlings at 13 or 40 weeks, when aggressive individuals adopted

mainly a LIW (83.9-100%) posture. Non-aggressive individuals at 1 week of age

assumed a more diverse range of postures than hatchlings at 13 or 40 weeks, when

HRH, and MA were the most common (Table 2).

Table 2. The percentage of agonistic interactions containing specific postures for

aggressive and non-aggressive hatchling C. porosus at 1, 13, and 40 weeks of age. As

MA can be displayed in conjunction with other postures during an agonistic

interaction, columns do not add to 100%. LIW = low in water; HTR = head and tail

raised; IP = Inflated posture; HRH = head raised high; MA = mouth agape.

1 week 13 weeks 40 weeks

aggressive

non

aggressive aggressive non aggressive aggressive

non

aggressive

Posture

LIW 50.0 40.2 83.9 32.8 100 43.8

HTR 16.7 17.4 1.7 1.7 0 0.0

IP 26.5 16.7 12.1 3.6 0 0.8

HRH 6.8 25.7 2.3 61.9 0 55.4

MA 3.8 0.8 1.1 25.3 0 38.3

5. Non-contact and Contact Movements

After assuming a posture, hatchlings often graduated to non-contact movements by

displaying a series of light jaw claps (LJC) with or without tail wagging (TW). LJCs

were used to indicate aggressive intent, while TW was also displayed by aggressive

individuals to forewarn (threaten) an impending contact movement. Non-aggressive

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individuals also engaged in TW in anticipation of an attack by an approaching

individual. TW often occurred after LJC, and increased in intensity as an interaction

escalated. The frequency of LJC displayed by aggressive individuals during an

interaction was highest among one week olds (F2,15 = 18.78, P < 0.05; Table 3). The

frequency of tail wagging (TW) was higher for aggressive (F2,15 = 4.01, P < 0.05) and

non aggressive (F2,15 = 4.98, P < 0.05) hatchlings at 1 week of age, and was not

displayed by aggressive individuals at 13 or 40 weeks of age (Table 3).

Contact movements were often adopted after non-contact movements, with TWB

and TWSHS (Figure 1h) being the most aggressive and intense forms. The frequency

of HP’s and B’s was significantly higher among 1 week olds (HP: F2,15 = 21.35, P <

0.05; B: F2,15 = 9.39, P < 0.05), as was the frequency of SHS’s and TWSHS’s (SHS:

F2,15 = 15.79, P < 0.05; TWSHS: F2,15 = 3.76, P < 0.05; Table 3). The frequency of

TWB’s was significantly lower among 1 week olds (F2,15 = 10.63, P < 0.05; Table 3).

The number of agonistic interactions in which contact was made was also lower

among 13 (66.2%) and 40 week old (45.5%) hatchlings (X2 = 106.06, df = 2, P <

0.05), compared with 1 week olds (94.5%). In many cases, the aggressive individual

made an unsuccessful attempt to bite the other animal that fled rapidly, thus avoiding

contact.

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Table 3. The number of different non-contact and contact movements incorporated

into the average agonistic interaction, by aggressive and non-aggressive C. porosus

hatchlings of different ages (1, 13 and 40 weeks). Any one agonistic interaction can

include multiple incidents of each type of movement. LJC = light jaw clap; TW = tail

wag; HP = head push; B = bite; TWB = tail wag bite; SHS = side head strike;

TWSHS = tail wag-side head strike.

1 week 13 weeks 40 weeks

aggressive

non

aggressive aggressive

non

aggressive aggressive

non

aggressive

mean ± se

Non contact

movements

LJC 0.75 ± 0.11 - 0.22 ± 0.04 - 0.02 ± 0.01 -

TW 0.14 ± 0.05 0.50 ± 0.09 0 0.54 ± 0.08 0 0.2 ± 0.02

Contact

movements

HP 0.49 ± 0.07 - 0.06 ± 0.01 - 0.11 ± 0.02 -

B 0.59 ± 0.06 - 0.25 ± 0.04 - 0.31 ± 0.05 -

TWB 0.18 ± 0.04 - 0.77 ± 0.09 - 0.83 ± 0.17 -

SHS 0.09 ± 0.04 - 0.06 ± 0.03 - 0.04 ± 0.01 -

TWSHS 0.40 ± 0.05 - 0.34 ± 0.07 - 0.03 ± 0.01 -

6. Intensity

While low intensity interactions appeared accidental, both medium and high intensity

interactions appeared deliberate. High intensity interactions were distinguished from

medium intensity interactions by the display of more intense contact movements, in

the form of TWB or TWSHS. The intensity of interactions differed among the age

cohorts (X2 = 166.66, df = 4, P < 0.05), with a decrease in low intensity interactions

among 13 and 40 week old hatchlings (Figure 3). There was also more high intensity

interactions at 13 weeks of age compared to 40 weeks of age. The majority of high

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intensity interactions occurred at dusk (1700-2000 h) and dawn (0600-0800h), while

low intensity interactions predominantly occurred during the night.

Figure 3. The overall percentage of agonistic interactions deemed to be low, medium

or high intensity, over a three night period (1700-0800 h), for C. porosus at 1 week

(a), 13 weeks (b) and 40 weeks (c) of age. All were housed in groups of 5 individuals

with 6 groups for each age class.

7. Duration and Outcome

The mean duration of an agonistic interaction was significantly longer among 1 week

old hatchlings (42.4 ± 2.60, 3 - 149 s; F2,15 = 1.97, P < 0.05) compared with 13 week

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old (22.1 ± 0.90 s, 6 - 59 s) and 40 week old hatchlings (17.6 ± 0.44 s, 5 - 41 s). In the

majority of interactions, the instigator was the winner, although this differed among

age cohorts. At 1 week 25% of instigators lost, whereas at 13 and 40 weeks only 0.6%

and 0.0% lost respectively.

The outcome of an agonistic interaction differed among the different age cohorts.

At 1 week, 56.8% of losers, defined as the least aggressive individual and the first to

back down, took flight slowly (SF; Figure 4), whereas by 13 and 40 weeks, 81.6%

and 100% of losers took flight rapidly (RF), and usually with the aggressive

individual giving chase (C) until the loser left the water (Figure 4).

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Figure 4. Percentage of C. porosus hatchlings involved in agonistic interactions that

ended in different outcomes at 1 week (a), 13 weeks (b) and 40 weeks (c) of age. All

were housed in groups of 5 individuals with 6 groups for each age cohort.

8. Clutch Specific Differences

A closer look at the ‘sibling only’ groups at one week of age revealed clutch specific

differences in the number of agonistic interactions (F5,12 = 4.0, P < 0.05) with a higher

frequency among groups 1, 3, and 4 compared with those in 5 and 6 (Figure 5).

Groups 1 and 3 also had a higher proportion of high intensity interactions (55%)

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compared with the other four groups (high intensity: < 25%; X2 = 25.44, df = 10, P <

0.05). While groups 3, 4, 5 all consisted of 4 male and 1 female, groups 1 and 6 had

no females. Consequently, the composition of each group with respect to sexes

present/absent does not correlate with the proportion of high intensity interactions

observed.

Figure 5. Mean number of agonistic interactions between hatchling C. porosus (N=5)

at one week of age in each of the six sibling only groups. Symbols distinguish

different sibling only groups.

Discussion

Within a few days of hatching, captive C. porosus hatchlings tolerate high levels of

close contact with each other, with little aggression, for most of the night. Yet at dusk

(1700-2000 h) and dawn (0600-0800 h), sporadic periods of agonistic interactions

occur between two individuals at any one time. Agonistic behaviour has never been

reported before among crocodiles of this age. During these interactions, hatchlings

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exhibited a diverse range of behaviour in the form of postures (N=5), non-contact

(N=6), and contact (N=5) movements, and often in combination (Table 1; Figure 1).

No specific vocalizations were noted to accompany these various behaviours, nor

were any sex specific differences apparent. However, the frequency and nature of

agonistic interactions, along with the type and pattern of behaviour displayed, differed

between the three age groups.

1. Agonistic Interactions

Among hatchling C. porosus at 1 week of age, agonistic interactions were not well-

defined, with a higher number of both low intensity interactions (Fig. 3), and

interactions in which both individuals engaged in aggression. These interactions were

longer in duration and more often involved physical contact and resulted in the

instigator losing. The full repertoire of behaviour (Table 1) was displayed by

hatchling C. porosus at this age, while there were also clutch specific differences in

the frequency of agonistic interactions, suggesting a genetic and, or maternal

component. A similar undefined pattern of behaviour, characterised by unstructured

interactions in which all individuals often display both aggressive and submissive

behaviour has also been reported in several species of birds (Drummond, 2001),

mammals (Bekoff et al., 1981; Smale et al., 1995), and other reptiles (Burghardt,

1977; Drummond, 2006) that exist in social groups shortly after birth.

Among hatchlings at 13 and 40 weeks of age, agonistic interactions were an

‘aggression-submission’ form of dominance relationship (Drummond, 2006), with a

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more defined pattern of behaviour, in which individuals had a distinct role as either a

dominant or a subordinate. Interactions were of a medium to high intensity and more

frequent, especially among 40 week old hatchlings, although the duration was shorter.

A number of the behaviours initially displayed among hatchlings at 1 week of age

were either rarely displayed, or no longer present among hatchlings at 13 and 40

weeks of age. Instead, most interactions were characterised by a dominant individual

approaching another in a series of rapid advances (RA) while remaining low in the

water (LIW), almost as if stalking prey. In response, the subordinate individual often

adopted a head raised high (HRH) posture, combined with mouth agape (MA) to

indicate submission before taking flight rapidly (RF). The dominant animal would

then chase (C) the subordinate, while attempting a bite (B), until the subordinate left

the water area. In contrast with one week old hatchlings, individuals at 13 and 40

weeks of age were also rarely observed lying together at any time. These results

support the theory that dispersal by hatchling C. porosus may be driven by a growing

intolerance of conspecifics (Webb & Messel, 1978).

2. Dominance Hierarchy

This study suggests that agonistic interactions between C. porosus immediately post-

hatching, when hatchlings would naturally exist together in crèches (Webb & Messel,

1978), may be important in the initial establishment of dominance. This pattern

appears to be a common strategy for many reptiles that exist in social groups for a

short period after birth (Burghardt, 1977; Stamps & Tanaka, 1981; Phillips et al.,

1993). Hatchling C. porosus are clearly born with the ability to display a wide range

103

of agonistic behaviour, but as they grow, these are replaced by a simpler subset of

behavioural interactions based on social status. When C. porosus in the wild would

naturally disperse around 13 weeks of age, subordinate individuals clearly recognise

aggression displayed by dominant individuals, and have learnt to avoid physical

contact (and thus potential injury) by indicating submission and by promptly fleeing.

At 40 weeks of age, C. porosus are much larger in size, and in the wild would be

largely solitary.

The development of agonistic interactions in hatchling C. porosus is indicative of

an increasingly well-defined dominance hierarchy in this species, characterised by a

clearly recognisable, asymmetrical pattern of aggression-submission interaction

(Drummond, 2006). This pattern of dominance, in which an aggressive display by one

individual elicits a submissive response without aggression in the other, has also been

reported in birds (Drummond, 2001), mammals (Smale et al., 1995; Bekoff et al.,

1981), and fish (Bergman, 1968), and appears typical for C. porosus in general based

on the limited information available (Messel et al., 1981; Lang, 1987; Riese, 1991;

Brien pers. observation).

Both Riese (1991) and Messel et al. (1981) report an almost identical dominance

pattern among hatchling C. porosus (3-50 weeks post hatch) in captivity and juvenile

and subadult C. porosus (90-240 cm total length) in the wild respectively, with most

interactions occurring in shallow water near the bank. In the majority of cases, the

dominant animal would approach low in the water, while the subordinate would

respond by raising the head up high, before fleeing rapidly with the dominant animal

104

giving chase. To escape, the subordinate individual often ran up on land, which

caused the dominant animal to cease chasing.

Although a number of species are equipped with the ability to inflict serious

damage and even death in conspecifics (eg. teeth, horns), this rarely occurs because

the majority have evolved strategies to minimize the chance of injury, which in most

cases takes the form of a dominance hierarchy (Carpenter & Ferguson, 1977;

Lumsden & Holldobler, 1983). This also appears to be the case in C. porosus, a

species with a formidable armoury that has long been regarded as the most aggressive

of all crocodilians (Lang, 1987). After hatchling C. porosus have dispersed from the

crèche (<13 weeks; Webb & Messel, 1978), they tend to be largely solitary and

nomadic as juveniles and sub-adults, and may only encounter other crocodiles

infrequently (Webb & Messel, 1978). As has been reported in lobsters (Huber &

Kravitz, 1995) and mice (Terranova et al., 1998), the early development of a defined

and clearly recognisable pattern of aggressive-submissive behaviour seems to enable

older C. porosus to resolve conflict rapidly and without injury when they do

encounter a conspecific.

The nature and ontogeny of agonistic behaviour and dominance hierarchies can

vary greatly both within and between taxa (Lovern & Jennssen, 2001; Drummond,

2006). Although little is known regarding agonistic behaviour and dominance in

crocodilians, a similar behavioural study involving captive Australian freshwater

crocodiles (C. johnstoni), a species regarded as gregarious and highly tolerant of

conspecifics, was recently undertaken (Brien et al., unpublished). In contrast to C.

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porosus, no such dominance hierarchy was present among C. johnstoni at 13 or 50

weeks of age. Typically, aggressive interactions between hatchling C. johnstoni were

also less frequent and intense, and less one-sided than in hatchling C. porosus, while

grouping was also common among C. johnstoni at 50 weeks of age. These differences

are likely due to distinct morphological and ecological differences between these

species, and further studies with other crocodilian species will likely demonstrate

further variation.

3. Territoriality

Sub-adult and adult C. porosus are known to be highly territorial, with larger

crocodiles often preventing smaller ones from accessing particular resources such as

basking sites, food, shelter and water (Lang, 1987; Grigg & Seebacher, 2000). While

agonistic interactions between hatchling C. porosus in this study often resulted in

temporary displacement, this did not result in hatchlings of any age being permanently

excluded from any area or resource (eg. food) within the enclosure. However, among

hatchling C. porosus at 13 and 40 weeks of age, shallow, open water areas appear to

be an important resource, with dominant individuals clearly attempting to exclude

others from it during periods of aggression (dusk and dawn).

Messel et al., 1981 also reported resident juvenile (90-240 cm total length) C. porosus

in the wild chasing conspecifics from areas of shallow water near the bank. Although

dependent largely upon the availability of resources, which can often be limited in

captivity, taken together, this indicates that territoriality may occur early in juvenile C.

porosus (Bustard and Maharana, 1983). It also suggests that shallow water near the

106

bank may be a critical resource, at least for smaller C. porosus, which is where they

tend to feed and would be less vulnerable to aquatic predators (Lang, 1987).

4. Agonistic Behaviour

The range of postures, non-contact, and contact movements displayed by hatchling C.

porosus is similar to those observed for juveniles and adults of other species of

crocodilian (Garrick & Lang, 1977; Vliet, 1989; Lang, 1987), including C. porosus

(Webb & Manolis, 1989; Brien pers. obs). This suggests that C. porosus, and possibly

most species of crocodilian, may have a pattern of signal or behavioural ontogeny

commonly seen in some lizards (Cooper, 1971; Stamps, 1978; Lovern & Jenssen,

2001), in which individuals are born with almost the full repertoire of agonistic

behaviour. While conditions experienced in captivity might expedite the onset and

development of agonistic behaviour in hatchling C. porosus, the results still illustrate

the potentially innate nature of agonistic behaviour in this species.

While a number of the behaviours displayed by hatchling C. porosus appear to be

standard forms of communication during agonistic interactions among crocodilians in

general, several also appear common in other taxa. The raising of the head up high on

an angle (HRH), or snout lifting (Garrick & Lang, 1977), is a clear indication of

submission in crocodilians, while raising or inflating the whole body (HTR, IP)

signals aggression (Garrick & Lang, 1977; Vliet, 1989; Senter, 2008). Raising or

inflating the body is commonly used by many taxa to indicate aggressive intent,

including lizards (Burghardt, 1977; Stamps, 1983), salamanders (Staub, 1993), and

107

crustaceans (Huber & Kravitz, 1995).

The clapping of the jaws together by crocodilians either lightly, in the case of

hatchling C. porosus, or as an intense event producing a loud noise in adults, is also

used to signal aggression (Garrick & Lang, 1977; Lang, 1987), while tail wagging

(TW) is often performed by subordinates and indicates stress or high agitation

(Garrick & Lang, 1977). In all crocodilians studied to date, both behaviours appear to

be graded signals, indicating differing degress of intensity, from low to high. Jaw

clapping, or snapping, also occurs in Plethodontid salamanders to signal aggressive

intent (Staub, 1993), while rapid twitching of the tail from side to side has been

reported in lizards (Carpenter et al., 1970; Torr & Shine, 1994), mice (Terranova et

al., 1998), and salamanders (Staub, 1993), to indicate high agitation or stress rather

than a ritualised social signal.

5. Management Implications

The presence of agonistic behaviour involving physical contact among hatchling C.

porosus at one week of age, along with clutch specific differences, has potentially

important implications for raising hatchling C. porosus in captivity. As with a number

of other species of reptiles (Carpenter & Ferguson, 1977; Phillips et al., 1993; Goetz

& Thomas, 1994; Worner, 2009), high levels of aggression may be responsible for

divergent patterns of growth among hatchling C. porosus in captivity, and may be

linked to lower survivorship among slow-growing animals (Bustard and Maharana,

1983; Isberg et al., 2009). If so, husbandry techniques that reduce the frequency of

108

agonistic interactions may improve growth and survival of hatchling C. porosus raised

for farming or conservation purposes.

Acknowledgements

We thank Chris Gienger, Jemeema Brien, and Charlie Manolis for their help in

different phases of the project. We would also like to thank Wildlife Management

International for the supply of animals, use of facilities, logistical support and major

funding for this project. WMI funding through the Rural Industries Research and

Development Corporation is gratefully acknowledged. Funding for cameras and

digital video recorders was provided through a Holsworth Wildlife Research

Endowment (ANZ Trustees Foundation), Northern Territory Research and Innovation

Board student grant, IUCN-SSC Crocodile Specialist Group Student Research

Assistance Scheme grant, and Charles Darwin University. Experimental protocols

were approved by the Charles Darwin University Animal Ethics Committee (Animal

ethics permit number A11003).

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Crocodylus porosus in Arnhem Land, northern Australia. – Copeia 1977: 238-

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Webb, G.J.W., Beal, M.A., Manolis, S.C. & Dempsey, K.E. (1987). The effects of

incubation temperature on sex determination and embryonic development rate

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119

Chapter 3.2. Intra- and interspecific agonistic behaviour in hatchling

Australian freshwater crocodiles (Crocodylus johnstoni) and


Published as: ‘Brien, M.L., Webb, G.J., Lang, J.W., McGuinness, K.A., Christian,

K.A. 2013. Intra- and interspecific agonistic behaviour in hatchling Australian

freshwater crocodiles (Crocodylus johnstoni) and saltwater crocodiles (Crocodylus

porosus). Australian Journal of Zoology 61: 196-205’. Formatted according to author


Abstract

We examined agonistic behaviour in hatchling Australian freshwater crocodiles

(Crocodylus johnstoni) at 2-weeks, 13-weeks, and 50 weeks after hatching, and

between C. johnstoni and saltwater crocodiles (Crocodylus porosus) at 40–50 weeks

of age. Among C. johnstoni, agonistic interactions (15–23 seconds duration) were

well established by two weeks old and typically involved two and occasionally three

individuals, mostly between 17:00–24:00 h in open water areas of enclosures. A range

of discrete postures, non-contact and contact movements are described. The head is

rarely targeted in contact movements with C. johnstoni because they exhibit a unique

‘head raised high’ posture, and engage in ‘push downs’. In contrast with C. porosus of

a similar age, agonistic interactions between C. johnstoni were conducted with

relatively low intensity, showed limited ontogenetic change, and there was no

evidence of a dominance hierarchy among hatchlings by 50 weeks of age, when the

frequency of agonistic interactions was lowest. Agonistic interactions between C.

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johnstoni and C. porosus at 40–50 weeks of age were mostly low level, with no real

exclusion or dominance observed. However, smaller individuals of both species

moved slowly out of the way when a larger individual of either species approached.

When medium or high level interspecific interactions did occur, it was between

similar-sized individuals, and each displayed species-specific behaviours that

appeared difficult for contestants to interpret: there was no clear winner of loser. The

nature of agonistic interactions between the two species suggests that dominance may

be governed more strongly by size rather than species-specific aggressiveness.

Introduction

Agonistic behaviour is any behaviour relating to aggression including threat, display,

attack, submission and flight (Tinbergen 1952; 1953; Wilson 1975). Agonistic

behaviour plays a crucial role in determining access to resources such as food, shelter

and mates in many species of bird (Drummond 2001), reptile (Phillips et al. 1993),

crustacean (Huber and Kravitz 1995), fish (Genner et al. 1999), and amphibian (Staub

1993). For many of these species, agonistic behaviour starts shortly after birth and is

important in the formation of dominance hierarchies and in determining future rates of

growth and survival (Tinbergen 1953; de Waal and Luttrell 1989; Drummond 2006).

Therefore, studies of agonistic behaviour during early development can greatly

improve our understanding of the social structuring and population dynamics of a

species.

The role of agonistic behaviour in interspecific competition is not as well

understood. It can be expected to occur between species that exist in sympatry and

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utilise similar resources (Brown and Wilson 1956; Ricklefs 1990), and may well

contribute to divergence in morphology, behaviour and ultimately niche partitioning

(Brown and Wilson 1956; Adams 2004), as proposed for mammals (Stoecker 1972;

Pereira and Kappeler 1997; Aguirre et al. 2002), birds (Schoener 1965; Murray 1971;

Smith 1990), salamanders (Jaeger 1972; Adams 2004), fish (Newman 1956) and

crustaceans (Bovbjerg 1970).

Knowledge of agonistic behaviour in crocodilians is mostly associated with adults

and breeding biology, in wild and captive situations (Cott 1961; Pooley 1969; Garrick

and Lang 1977; Garrick et al. 1978; Vliet 1989; Thorbjarnarson 1991). With

saltwater crocodiles (Crocodylus porosus), which are considered the most aggressive

of extant crocodilian species (Lang 1987), they begin life in hatchling crèches and

dominance hierarchies become established within the first three weeks of life (Brien

et al. 2013). Intolerance of conspecifics has long been implicated in their dispersal

from crèches after a few months, and in the later spatial separation of juveniles and

adults (Webb et al. 1977; Messel et al. 1981; Lang 1987). The degree to which

agonistic behaviour occurs in less aggressive crocodilian species is unknown.

Australian freshwater crocodiles (Crocodylus johnstoni) are regarded as one of the

least aggressive crocodilians (Lang 1987). Like C. porosus, they exist in crèches after

hatching, but unlike C. porosus, juvenile and adult C. johnstoni often congregate at

high densities during the annual dry season (Webb et al. 1983a; Kennett and Christian

1993). They thus appear much more tolerant of conspecifics, although some discrete

behaviours such as tail raking, are implicated in dominance hierarchies (Webb et al.

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1983c). Although C. johnstoni and C. porosus have largely allopatric distributions in

northern Australia, they also coexist within zones of sympatry in some rivers and

wetlands (Webb et al. 1983a). Despite the larger size of adult C. porosus, and the

strong possibility that adult C. porosus may control C. johnstoni populations in such

zones (Webb et al. 1983a), juveniles of each species live together with similar size-

specific morphology, diet and spatial needs (Messel et al. 1981; Webb et al. 1983a),

which is reasonably uncommon in situations where crocodilian distributions overlap

(Ouboter 1996; Thorbjarnarson et al. 2006).

The present study was undertaken with two primary aims. Firstly, to describe

agonistic behaviour in hatchling C. johnstoni, and determine whether the nature and

ontogeny is similar to that observed in hatchling C. porosus (Brien et al. 2013).

Secondly, to examine how C. johnstoni and C. porosus respond during agonistic

interactions involving both species.

Materials and methods

Subjects and housing

In December 2011, 70 hatchling Australian freshwater crocodiles (Crocodylus

johnstoni), in three age cohorts, were provided by Wildlife Management International

(WMI; Darwin, Australia). All had been captured in the wild from crèches when <1

week post-hatching (based on size and extent of yolk scar healing), and were almost

certainly siblings. The first cohort (n = 25) contained individuals from five different

clutches (20 males, 5 females), two weeks after hatching, while the second (13 weeks

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after hatching; n = 25; 19 males, 6 females) and third (50 weeks after hatching; n =

25; 20 males, 5 females) cohorts contained hatchlings from a further six and seven

different clutches respectively, that were of similar size and age. These age cohorts

were based on the early life history of C. johnstoni which is similar to that described

for C. porosus (Brien et al. 2013). This also enabled direct comparisons. Using the

same crocodiles throughout the study was initially considered but not feasible, due to

the highly variable nature of growth within and between different clutches for this

species and crocodilians in general, which can lead to significant differences in size

and high rates of mortality during the first year of life under captive conditions (Webb

et al. 1983b; Brien et al. 2013).

Hatchling C. johnstoni of different ages were transferred to experimental

enclosures and housed in groups of five individuals for the duration of the study. For

each animal, snout-vent length (SVL to the front of the cloaca - mm), total length (TL

in mm), and body mass (BM in g) were measured and a uniquely numbered metal

webbing tag (Small animal tag 1005-3, National Band and Tag Co.) was attached to

the rear back right foot. Mean size of crocodiles at the initiation of observations were:

2-week olds, 110.5 ± 0.5 mm SVL, 245.3 ± 1.1 mm TL, and 42.7 ± 0.8 g mass; 13-

week olds, 147.0 ± 1.7 mm SVL, 316.8 ± 2.8 mm TL and 76.3 ± 1.8 g mass; 50 week

olds, 305.5 ± 1.7 mm SVL, 618.8 ± 2.3 mm TL, and 628.2 ± 14.5 g mass.

In February 2012, 12 hatchling C. porosus at 40 weeks after hatching (10 male, 2

female) and 12 hatchling C. johnstoni of a similar size and age (50 week after

hatching, 9 male, 3 female) were also provided by WMI. However, while the three

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age cohorts of C. johnstoni were all captured from the wild, the 40 week old C.

porosus were from seven different clutches of eggs artificially incubated in captivity

(see Brien et al. 2013). In the wild, this is the age and, or size at which C. johnstoni

and C. porosus are naturally found occupying similar habitat (Webb et al. 1983a).

Hatchlings of both species were transferred to experimental enclosures and housed in

six groups of four individuals (2 C. porosus and 2 C. johnstoni), each containing two

similar size ‘large’ crocodiles of each species (CJ: 345.2 ± 3.7 mm SVL, 700.5 ± 7.4

mm TL, 957.2 ± 34.7 g mass; CP: 348.8 ± 3.1 mm SVL, 709.7 ± 6.7 mm TL, 952.2 ±

24.8 g mass) and two similar size ‘small’ crocodiles of each species (CJ: 305.5 ± 1.7

mm SVL, 618.8 ± 2.3 mm TL, 628.2 ± 14.5 g mass; CP: 300.3 ± 2.8 mm SVL, 624.0

± 3.9 mm TL, 632.2 ± 10.8 g mass).

The fibreglass enclosures in which the experimental groups (C. johnstoni only, C.

johnstoni and C. porosus combined) were housed were box shaped (170 x 100 x 50

cm), with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x

100 cm; < 8 cm deep). Therefore, all hatchlings were at a density of 2.9 animals per

m2 which was considered very low based on previous studies (Riese 1991; Mayer

1998). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided in each

enclosure, and was constructed with eight lengths of PVC pipe (80 cm long; 10 cm

diameter) strapped together and on legs, centrally positioned in the water (partly

immersed) and overhanging the land. Water temperatures were maintained at 30–

32°C, and air temperatures varied from 26–32°C, with a natural light cycle. All

animals were fed chopped red meat supplemented with di-calcium phosphate (4%)

and a multivitamin supplement (1%), which is the standard diet fed to hatchling C.

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johnstoni and C. porosus in captivity. Enough food for each individual was made

available throughout the night (16:00–17:00 h), which is when hatchling C. johnstoni

and C. porosus are known to feed in captivity and in the wild (Lang 1987; Brien et al.

2013). Waste removal and cleaning occurred the following morning (08:00–09:00 h)

when the water was changed. Hatchlings of both species were subject to the same

raising conditions (enclosure, temperature, density, and husbandry) prior to, and

during the experiments.

Recording behaviour


record all behaviour on digital video recorders (Signet 4CH QV–8104). For the three

cohorts of C. johnstoni, a recording period lasted 15 hours (17:00–08:00 h), and was

conducted on three consecutive nights for each group (45 h per group). To allow for

settling, the recordings were taken 4–5 days after the crocodiles were placed in the

new experimental enclosures. This night-time sampling period was based on previous

recordings (100’s of hours) that revealed no agonistic behaviour in C. johnstoni

hatchlings between 08:00 and 17:00 h, when they were inactive and under cover. For

the mixed species groups, recordings were only taken during the first two nights

(17:00–08:00 h) when, from previous experience, the level of aggression and

frequency of interactions is typically high. Despite the documented importance of

vocalisations during crocodilian communication at all life stages (Lang 1987),

especially among hatchlings and juveniles, no audio was recorded during this study

due to limitations of the recording equipment.

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Agonistic interactions


aggression and intolerance appeared to be signalled by postures or actions by one or

more individuals. An aggressive individual was one that made deliberate advances

toward another, or that made physical contact with another. Each agonistic interaction

was described in terms of whether one or both contestants engaged in aggression, and

the intensity (low, medium, high) demonstrated. Low intensity interactions appeared

accidental, occurring when individuals lying together disturbed each other when

moving, or if one swam into another underwater. Medium and high intensity

interactions appeared deliberate, with one individual approaching another with the

apparent goal of initiating an agonistic interaction. High intensity interactions were

distinguished from medium intensity interactions by the display of more intense

contact behaviours. The behaviour exhibited, the intensity of interaction (low,

medium, high), the location (water, hide, land), the time, duration of interaction and

outcome were all obtained from the videos, as previously described for C. porosus

(Brien et al. 2013).

Classification of behaviour


inventory of agonistic behaviours for C. johnstoni hatchlings, similar to that described

for hatchling C. porosus (Brien et al. 2013). The descriptions are based on a series of

basic postures, modified by movement of body parts, or of the whole animal, and

whether visual signals or actual contact was involved. Some of these behaviours have

been described in studies with adult crocodilians (Garrick and Lang 1977; Lang

127

1987).



Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro–


repeated-measures ANOVA was used for comparison of means between 2-, 13-, and

50-week-old hatchlings, with consecutive night of recording (N = 3) as the repeated

measure. A Pearsons’ Chi-square test was used to compare intensity, outcome, contact

made, number of individuals being aggressive, and how often the instigator won,

where sample sizes were adequate. To test whether variation in the frequency of

interactions could be explained by time of day, the results were grouped into one of

three periods: dusk 17:00–20:00 h; night 20:00–06:00 h; and dawn 06:00–08:00 h. A

significance level of P < 0.05 was used for all statistical tests. All means are reported

± one standard error with sample sizes.

Results

The majority of agonistic interactions between hatchling C. johnstoni involved two

individuals in open water, with none observed on the land or near food (on land).

However, there were two interactions at 13 weeks and three at 50 weeks in which 3–4

individuals were involved in an agonistic interaction. Some interactions appeared to

occur accidentally when individuals lying together disturbed each other when moving

off, or if one swam into another underwater. However, interactions were also initiated

either by one or both individuals moving toward each other in a series of short, rapid,

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deliberate advance movements (RA). In response to RA, one or both individuals

would adopt a series of other agonistic behaviours that involved the adoption of some

discrete postures that varied in the intensity of expression (Table 1; Fig. 1).

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Table 1. Classification of the behaviour used by hatchling C. johnstoni during

agonistic interactions. Responses to aggression can be graded, involving the adoption

of static postures, followed by non-contact movements followed again by contact

movements. This table has been adapted from Brien et al. 2013. * = has not been

previously described, or is different in some way.


Initiation

Rapid advance RA Series of short rapid advance movements towards

another individual while LIW.

Termination

Slow flight SF Slow movement away from another individual in a

LIW posture.

Rapid flight RF Rapid movement away from another individual in a

LIW posture.

Posture

Low in water LIW Immobile with only the top of the head and back

above the water surface.

Head raised high HRH* Immobile with upward extension of the head high

out of the water on a ~45º angle while tail remains

low. However, unlike C. porosus, body remains low

in water.

Mouth agape MA Immobile with mouth opened wide (in combination

with postures LIW, IP, HTR or HRH).

Non-contact movement

Light jaw–clap LJC Rapid opening and closing of the jaws at the water

surface, often repeated several times (LIW posture).

Tail–wagging TW Undulation of the tail from side to side in either a

gentle sweeping motion or rapid twitching, often

repeated several times (all postures).

Contact movement

Head push HP Head is pushed in to an opponent, usually with

mouth closed (LIW posture).

Push down PD* Chest and neck of individual pushed down on the

upper neck or back of an opponent (HRH posture).


Side head-strike SHS Head is thrust sideways in to an opponent while the

mouth is either open or closed (all postures).

Tail–wag bite TWB Tail wagging occurs prior to a bite and propels the

individual into an opponent with force (LIW

posture).

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Figure 1. Push down (PD) contact movement (a) displayed exclusively by hatchling

C. johnstoni during agonistic interactions and head raised while resting (non-

aggressive) (b) at 2 weeks, 13 weeks and 50 weeks of age, described in Table 1.

The adoption of such postures could be abandoned at any time by either slow (SF)

or rapid flight (RF), ending the agonistic interaction. Alternatively, the signals

emanating from the postures could be intensified with body movements, such as light

jaw claps (LJC) or tail wagging (TW), which were displays not involving physical

contact with combatants. If the interaction was still not terminated by flight of one or

both animals, the behaviour intensified further, with contact movements such as head

pushing (HP), or biting (B), occasionally combined in different ways with intense tail

wagging (TWB), or side head striking (SHS), until one or both individuals took flight.

Another contact movement unique to C. johnstoni was a push down (PD) (Fig. 1).

When crocodiles were not engaged in aggression and were at rest, they typically lay

with their head raised up on an angle, appearing as if on look out (Fig. 1).

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Aggression

An aggressive individual was defined as one that made deliberate advances toward

another and, or which made physical contact with another animal. Each agonistic


aggression, and whether this differed across age classes. The number of interactions in

which both individuals appeared aggressive was similar for all age classes (X2 = 2.48,

df = 2, P > 0.05), with 31.7% at 2 weeks, 41.2% at 13 weeks and 40% at 50 weeks.

The number of separate movements or steps in the RA did not change significantly

with age (F2,12 = 1.04, P > 0.05), with a mean of 1.9 ± 0.10 steps (mean of means;

range 0–4; n = 15) per interaction.

Frequency

The mean number of agonistic interactions per group per night at two weeks of age

was 6.9 ± 0.42 (mean of means; n = 5, range 5–10). The frequency of agonistic

interactions was significantly lower among the older age cohorts (F2,10 = 20.55, P <

0.05), with 5.7 ± 0.35 (n = 5, range 4-9) at 13 weeks, and 2.8 ± 0.86 (n = 5, range 2–5)

at 50 weeks.

Timing

For all three age cohorts combined, the frequency of agonistic interactions at dusk

(17:00–20:00 h), night (20:00–06:00 h) and dawn (06:00–08:00 h) varied significantly

(F2,11 = 6.99, P < 0.05). The majority of agonistic interactions occurred throughout the

night (17:00–02:00 h), and were lower during the early morning (Fig. 2). Outside of

agonistic interactions, hatchlings of all ages would often lie together in contact, in the

132

water, in groups of 2–5 individuals. The 2- and 13-week-old hatchlings would retreat

under the hide and were rarely visible after 06:00 h.

Figure 2. Percentage of agonistic interactions (%) as a function of hour (17:00–08:00 h) for

C. johnstoni housed in groups of 5 at three different ages (2, 13 and 50 weeks).

Postures

The postures displayed in agonistic interactions, as deemed to be aggressive and non-

aggressive, varied among the three age cohorts (Table 2). At two weeks old, all

hatchlings typically remained LIW (~80%) during an interaction (Table 2). The

number of aggressive hatchlings observed in an HRH posture during an agonistic

interaction was significantly higher among the older age cohorts (X2 = 29.06, df = 2, P

< 0.05), while the number of non-aggressive individuals observed in an HRH posture

during an interaction was highest among 50-week-olds (X2 = 10.39, df = 2, P < 0.05;

Table 2). The number of hatchlings with MA was higher among the older age cohorts

for both aggressive and non-aggressive individuals (Table 2).

133

Table 2. The percentage of agonistic interactions containing specific postures for

hatchling C. johnstoni at 2, 13 and 50 weeks of age deemed aggressive and non-

aggressive. As MA can be displayed in conjunction with other postures during an

agonistic interaction, columns do not add up to 100%. LIW, low in water; HRH, head

raised high; MA, mouth agape.

Posture 2 weeks 13 weeks 50 weeks

Aggressive Non-

aggressive

Aggressive Non-

aggressive

Aggressive Non-

aggressive

LIW 82.5 80.3 63.3 88.8 45.0 56.0

HRH 17.5 19.7 36.7 12.0 55.0 44.0

MA 0 1.4 2.5 8 8.3 12.0

Non-contact and contact movements

After assuming a posture, hatchlings often graduated to non-contact movements by

displaying a series of LJC’s with or without TW. LJCs appeared to indicate

aggressive intent, while TW was also displayed by aggressive individuals and

appeared to forewarn (threaten) of an impending contact movement. Non-aggressive

individuals also engaged in TW which appeared to signal anticipation of an attack by

an approaching individual. TW often occurred after LJC, and increased in intensity as

an interaction escalated. LJC’s were only displayed by aggressive individuals at two

weeks of age, while the display of TW by aggressive and non-aggressive individuals,

despite being infrequent, was displayed at both two weeks and 50 weeks of age (Table

3).

Contact movements were often adopted after non-contact movements. The

frequency of HP’s was significantly higher at two weeks of age (F2,12 = 3.60, P <

0.05), while the frequency of PD’s was slightly higher at 13 and 50 weeks of age

(F2,12 = 0.76, P < 0.05; Table 3). The frequency of B’s was similar for all age cohorts

134

(F2,12 = 0.34, P > 0.05), while SHS’s were infrequent (Table 3). The number of

agonistic interactions in which contact was made did not change significantly with

age (X2 = 0.70, df = 2, P > 0.05), with an average of 90% for all three age groups (2

weeks: 92.7%; 13 weeks: 92.5%; 50 weeks: 90.3%).

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Table 3. The number of different non-contact and contact movements incorporated into the average agonistic interaction, by aggressive and non-

aggressive C. johnstoni hatchlings of different ages (2-, 13-, 50-weeks-old). Any one agonistic interaction can include multiple incidents of each

type of movement. LJC, light jaw clap; TW, tail wag; HP, head push; B, bite; PD, push down; SHS, side head strike. For each measure mean ±

SE is presented.

Movement 2 weeks 13 weeks 50 weeks

Aggressive Non-

aggressive

Aggressive Non-

aggressive

Aggressive Non-

aggressive

Non contact movements

LJC 0.30 ± 0.06 - 0 - 0 -

TW 0.03 ± 0.02 0.05 ± 0.03 0 0.04 ± 0.03 0.03 ± 0.03 0.07 ± 0.07

Contact movements

HP 0.91 ± 0.09 - 0.30 ± 0.03 - 0.20 ± 0.06 -

PD 0.07 ± 0.02 - 0.23 ± 0.03 - 0.55 ± 0.19 -

B 0.91 ± 0.12 - 0.61 ± 0.05 - 0.88 ± 0.15 -

SHS 0.07 ± 0.03 - 0.02 ± 0.01 - 0.07 ± 0.05 -

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Intensity

While low intensity interactions appeared accidental by definition, both medium and

high intensity interactions appeared deliberate. High intensity interactions were

distinguished from medium intensity interactions by the display of more intense

contact movements, in the form of TWB. The majority of interactions between

hatchlings of all ages were mostly low or medium intensity, with only two high level

interactions observed between hatchlings at 50-weeks-old. The proportion of low and

medium level interactions did not differ with age (X2 = 2.98, df = 2, P > 0.05).

Duration and outcome

The mean duration of an agonistic interaction was similar between two week (16.1 ±

1.32 s, 5–120 s) 13 week (15.6 ± 0.97 s, 5–50 s) and 50-week-old hatchlings (23.0 ±

3.3 s, 6–88 s) (F2,12 = 0.31, P > 0.05). The instigator in the majority of agonistic

interactions was usually the winner, and this did not change with age (X2 = 2.14, df =

2, P > 0.05).

The outcome of an agonistic interaction did not differ between the three age groups

(X2 = 19.85, df = 8, P > 0.05). The most common outcome was that both individuals

stood their ground (37.7%), or the loser, defined as the least aggressive individual and

the first to back down, took flight slowly (SF: 27.7%). Very few interactions (4.5%)

resulted in the loser taking flight rapidly (RF).

Interspecific agonistic interactions

Among groups containing hatchling C. johnstoni (1 small, 1 large) and C. porosus (1

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small, 1 large) of a similar size and age, a mean of 11.2 ± 1.2 (mean of means, range

8-16) agonistic interactions was observed mostly (46.3%) around dusk (17:00-20:00

h). The majority of these interactions (74%) were low intensity and involved both

species and sizes, with biting the most common behaviour (92.4%). Individuals of

both species were commonly observed lying together or near each other, with no

obvious partitioning, exclusion or dominance observed. However, size did vary within

groups and if a larger animal approached a smaller one, regardless of species, the

smaller individual would move slowly out of the way in response. There was also a

clear distinction between the two species while at rest, with C. porosus remaining

LIW and C. johnstoni lying with the head raised (Fig. 1).

The few medium and high intensity agonistic interactions observed occurred

between individuals of the same size (different species). During these interactions,

individuals displayed a species-specific pattern of behaviour, described for C.

johnstoni at 50-weeks-old in this study, and for C. porosus at 40-weeks-old in Brien et

al (2013). The typical pattern involved C. porosus rapidly advancing (RA) towards C.

johnstoni. However, unlike agonistic interactions between two C. porosus, where this

behaviour clearly signals dominance and elicits rapid flight (RF) in the other animal,

C. johnstoni would stand its ground and appeared unclear about the intended message.

In some cases, due to the lack of response in C. johnstoni, the interaction would end.

However, if C. porosus continued to RA, C. johnstoni would respond by lifting its

head high in the air (HRH). The interaction would then escalate with C. porosus

remaining low in the water (LIW), biting (B) and side head striking (SHS), while C.

johnstoni would push down (PD) on the top of C. porosus and occasionally bite (B).

138

This resulted in the two individuals moving together in a circular motion and

becoming entangled. Both individuals appeared confused by this species–specific

behaviour, and the interaction would end with both lying together, often entangled, or

swimming away slowly with no clear winner.

Discussion

Within two weeks post–hatching, captive C. johnstoni hatchlings tolerated high levels

of close contact with each other with little evidence of aggression. C. johnstoni at all

ages (2-, 13-, and 50-weeks-old) regularly grouped together throughout the evening.

Agonistic interactions typically involved contact between two or more individuals, but

were of low intensity, and halved in frequency by the end of the first year. Clear

dominance or submissive outcomes from an interaction were infrequent, and there

was no evidence of a dominance hierarchy within groups by 50 weeks of age.

Agonistic behaviour

Hatchling C. johnstoni exhibited a diverse repertoire of postures (n = 3), non-contact

movements (n = 5) and contact movements (n = 6) that were utilized in agonistic

interactions. All of these behaviours were displayed by individuals at two weeks of

age, and most were utilized in similar contexts, with few ontogenetic changes during

the first year of life. None of the behaviours appeared to be sex specific, and while

vocalisations may play an important role in agonistic interactions, audio was not

recorded in this study. One behaviour, a push-down contact movement (=PD) in C.

johnstoni has never been observed in C. porosus hatchlings under the same

conditions. The other 13 behaviour components listed in Table 4 were shared between

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the two species.

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Table 4. Comparison of the behavioural repertoire of hatchling C. johnstoni and C. porosus during agonistic interactions at various stages (in

weeks) to illustrate shared and species-specific behaviours, and ontogenetic changes. N: neutral, behaviour equally likely to be aggressive or

submissive; A: aggressive, behaviour by aggressive animal; S: submissive, behaviour by submissive individual; ( ): parentheses indicate

behaviour performed at low frequency or rarely observed.

C. porosus C. johnstoni

Agonistic

behaviour

Present

in both

species

Hatchling age

Change in

behaviour

with age

Hatchling age

Change in

behaviour with

age

1

week

13

weeks

40

weeks

2

weeks

13

weeks

50

weeks

Posture

LIW Yes N A A increase N N N decrease

IP No N A absent decrease

HTR No N (N) absent decrease

HRH Yes (S) S S increase N (A) N increase

MA Yes A S S increase N (S) N increase

Non-contact movement

RA Yes A A A increase A A A same

SF Yes N S (S) decrease N N S same

141

RF Yes N (S) S increase (N) (N) (N) same

LJC Yes A A (A) decrease (A) absent absent decrease

TW Yes N S (S) decrease (N) (N) (N) same

Contact movement

HP Yes A A A decrease A A (A) decrease

PD No (A) A A increase

B Yes A A A decrease A A A same

SHS Yes (A) (A) (A) same (A) (A) (A) same

TWSHS No A A (A) decrease

TWB Yes A A A increase (A) (A) (A) increase

142

Lying either on land or in water with the head raised up at an angle (approx. 30º)

was commonly observed among C. johnstoni. This posture, not associated with

agonistic behaviour, makes them appear as if they are on ‘look out’. This behaviour

has been observed for C. johnstoni hatchlings in the wild (Somaweera pers. comm.),

and may indicate a heightened vigilance in a species that remains small and more

vulnerable to predation and inter-specific competition for an extended period. It was

not observed in C. porosus which tend to remain low in the water (LIW) while at rest


Push downs (PD) were displayed by either one or both C. johnstoni during an

agonistic interaction with a head raised high (HRH) posture, with hatchlings often

moving together in a circling motion as they attempted to push each other down. This

behaviour increased in frequency by 13 and 50 weeks of age and is very similar to

what has been reported for several species of salamander (Staub 1993; Davis 2002)

and snakes (Carpenter 1977), with the apparent aim of pinning the other individual

down in a ritualized display of dominance (Staub 1993; Davis 2002).

Raising the head, or ‘snout lifting’, has been reported among larger sub-adults and

adults of several crocodilian species, including C. johnstoni and C. porosus (Webb

and Manolis 1989), as a typical submissive response common to most species studied

to date (Lang 1987). It appears that the raising of the head and, or trunk may also

initially be an attempt at bluffing an opponent, but with age, signals submission. The

transition appears to occur more rapidly in hatchling C. porosus than in C. johnstoni

143


C. johnstoni rarely targeted the head of another individual during an interaction,

and often raised the head out of the way (HRH posture), especially when both

individuals were aggressive. This tendency to avoid contact with the head and the

prevalence of less injurious forms of contact (HP and PD) among C. johnstoni,

especially as they get older, may be linked to skull morphology. During the initial

post-hatching period, the shape of the snout in C. johnstoni is not noticeably different

to that of C. porosus, and the frequency of agonistic interactions and behaviours used

is similar (Brien et al. 2013). However, as C. johnstoni grow, the snout becomes

considerably narrower which coincides with a decrease in the frequency of agonistic

interactions and an increase in the frequency of push downs (PD) and head pushes

(HP).

As the long, narrow snouts of crocodilian species such as C. johnstoni are

structurally weaker than those of species with broader snouts (e.g. C. porosus)

(McHenry et al. 2006; Pierce et al. 2008), this makes them more vulnerable to broken

or damaged jaws during conflict (Huchzermeyer 2003), which can impair or prevent

their ability to feed or even be fatal (Webb et al. 1983c). The use of less invasive

contact behaviours and avoidance of the head may both have an adaptive evolutionary

significance in C. johnstoni, and perhaps with other slender-snouted species of

crocodilian which are often specialist fish eaters (Lang 1987).

Intraspecific agonistic interactions

144

The frequency and nature of agonistic interactions between C. johnstoni at two weeks

of age was similar to those seen between C. porosus hatchlings at 1 week of age,

when both species were maintained in captivity under comparable conditions (Brien et

al. 2013). In C. johnstoni, agonistic interactions decreased in frequency slightly by 13

weeks, and were reduced to less than one half of the initial frequency by 50 weeks.

Agonistic interactions involved contact (>90%) occurred at all ages, but were

typically two-sided and symmetrical, with each individual engaging in the same

behaviour, e.g., push-downs (=PD).

Interactions between hatchling C. johnstoni occurred largely between 17:00–

24:00h, with individuals at two and 13 weeks of age retreating under the hide boards

by 06:00h and not being seen again. In comparison, hatchling C. porosus of all ages

(1, 13, 40 weeks), had a characteristic dusk (17:00–20:00 h) and dawn (06:00–08:00

h) pattern of agonistic interactions and were regularly observed out in open areas <

08:00h. That hatchling C. johnstoni would retreat under the hide almost an hour

before sunrise, may again be linked to the greater vulnerability of hatchling C.

johnstoni to predation due to their smaller size.

Agonistic interactions between hatchling C. johnstoni typically involved two

individuals, and on occasion even up to three or four at 13 and 50 weeks of age. The

number of interactions in which both individuals were aggressive increased slightly

with age (30–40 % of interactions), as did the duration of an interaction, while the

number of times contact was actually made did not change (90% of interactions).

Almost all interactions between hatchling C. johnstoni were a low to medium

145

intensity, while the outcome varied, often resulting in either both individuals standing

their ground or the loser taking flight slowly. While the majority of interactions

resulted in the instigator winning (76.4%), this was far lower than for hatchling C.

porosus older than one week old (Brien et al. 2013).

The formation of dominance hierarchies is often important in limiting the cost of

interactions in species that exist together in social groups, while in more solitary

species, dominance is usually absent and individuals will engage in higher levels of

aggression (Bekoff 1974; 1977; Huntington and Turner 1987; Krause and Ruxton

2002). Although C. johnstoni in the wild are generally solitary, in some habitats they

are often forced to live together at higher densities during certain times of the year due

to lower water levels (Webb et al. 1983a), while they also show a high degree of site

fidelity and communal nesting (Webb et al. 1983a; Tucker et al. 1997).

While there was no evidence of a dominance hierarchy among C. johnstoni by 50

weeks of age in this study, agonistic interactions were relatively infrequent and of a

lower intensity, which may reflect a different social strategy enabling them to coexist

at certain times of the year. In comparison, C. porosus under captive conditions had

well-defined dominance hierarchies despite being largely solitary in the wild. While it

is possible that these results are a consequence of captivity, and that dominance may

develop at a later stage in C. johnstoni, it does indicate that juveniles of these two

species employ very different social strategies.

Interspecific agonistic interactions

146

Agonistic interactions between C. johnstoni and C. porosus in this study involved

only two individuals and were mostly low level, with no real exclusion or dominance

observed. However, smaller individuals of both species moved slowly out of the way

when a larger individual approached. Occasional medium or high level interactions

occurred between the same sized (different species) individuals in a group, and

involved both individuals displaying a species–specific pattern of behaviour with no

clear winner of the contest.

These results were unexpected, as observations of intraspecific aggression

suggested that C. porosus would dominate C. johnstoni due to a higher level of

aggression, and the use of more injurious forms of contact. Instead, it suggests that

interspecific interactions between these two species may be governed largely by size,

which has also been found among different species of crayfish (Vorburger and Ribi

2001) and trout (Newman 1956) during staged interactions. Given that C. porosus

reaches a much larger adult size, it is likely that C. johnstoni may avoid C. porosus in

the wild.

Since the recovery of the saltwater crocodile population in the Northern Territory

from hunting (Fukuda et al. 2011), there appears to have been displacement of C.

johnstoni by C. porosus from areas they previously occupied (Messel et al. 1981;

Webb et al. 1983a). Increased numbers of C. porosus were found to be negatively

correlated with C. johnstoni abundance, suggesting competitive exclusion (Messel et

al. 1981; Webb et al. 1983a). This situation has also been described in a number of

sympatric species of lizards (Jenssen 1973), salamanders (Jaeger 1972; Keen and

147

Sharp 1984), birds (Williams and Batzli 1979) and mammals (Terman 1974), with

removal of the competitively superior species resulting in increased habitat use by the

inferior one.

This study describes agonistic behaviour in C. johnstoni for the first time and

provides new insights into the nature of agonistic behaviour between C. porosus and

C. johnstoni at one year of age, a time at which they would naturally start occurring

together in the wild. Several clear differences exist in morphology, resource use, and

behaviour, between C. porosus and C. johnstoni, which may have been shaped by

interspecific agonistic interactions. As the larger, more dominant species, C. porosus

may have played a significant role in this divergent evolution.

Acknowledgements

We thank Charlie Manolis, Ruchira Somaweera, and Jemeema Brien for their help in

different phases of the project. We would also like to thank Wildlife Management

International for the supply of animals, use of facilities and logistical support. WMI

funding through the Rural Industries Research and Development Corporation is

gratefully acknowledged. Funding for equipment (cameras, digital video recorders)

was provided through a Holsworth Wildlife Research Endowment (ANZ Trustees

Foundation), a Northern Territory Research and Innovation Board student grant, an

IUCN Crocodile Specialist Group student grant, and Charles Darwin University.

Experimental protocols were approved by the Charles Darwin University Animal

Ethics Committee (Animal ethics permit number A11003).

148

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Chapter 3.3. The good, the bad, and the ugly: agonistic behaviour in

juvenile crocodilians

Published as: ‘Brien, M.L., Lang, J.W., Webb, G.W., Stevenson, C., Christian, K.A.

2013. The good, the bad, and the ugly: agonistic behaviour in juvenile crocodilians.

PloS one 8: DOI: 10.1371/journal.pone.0080872’. Formatted according to author


Abstract

We examined agonistic behaviour in seven species of hatchling and juvenile

crocodilians held in small groups (N = 4) under similar laboratory conditions.

Agonistic interactions occurred in all seven species, typically involved two

individuals, were short in duration (5-15 seconds), and occurred between 1600-2200 h

in open water. The nature and extent of agonistic interactions, the behaviours

displayed, and the level of conspecific tolerance varied among species. Discrete

postures, non-contact and contact movements are described. Three of these were

species-specific: push downs by C. johnstoni; inflated tail sweeping by C.

novaeguineae; and, side head striking combined with tail wagging by C. porosus. The

two long-snouted species (C. johnstoni and G. gangeticus) avoided contact involving

the head and often raised the head up out of the way during agonistic interactions.

Several behaviours not associated with aggression are also described, including snout

rubbing, raising the head up high while at rest, and the use of vocalizations. The two

most aggressive species (C. porosus, C. novaeguineae) appeared to form dominance

158

hierarchies, whereas the less aggressive species did not. Interspecific differences in

agonistic behaviour may reflect evolutionary divergence associated with morphology,

ecology, general life history and responses to interspecific conflict in areas where

multiple species have co-existed. Understanding species-specific traits in agonistic

behaviour and social tolerance has implications for the controlled raising of different

species of hatchlings for conservation, management or production purposes.

Introduction

Agonistic behaviour plays an important role in determining access to resources such

as food, shelter and mates, and in establishing dominance status in a wide range of

mammals [1] [2], birds [3] [4], fish [5] [6], reptiles [7] [8], amphibians [9] [10], and

invertebrates [11] [12]. Agonistic behaviour is often present shortly after birth or

hatching, and can vary widely in terms of the nature and ontogeny, both within and

among species [13]. This variability is often associated with differences in the

ecology, morphology, or general life history of a particular species or population,

which can have an evolutionary or adaptive significance [14] [15].

Among reptiles, many behaviours are largely considered ‘hard wired’ from birth,

because they are stereotypical in many species of lizard [8] [16], snake [7] [17],

crocodilian [18] [19] and possibly chelonian [20]. However, detailed information on

agonistic behaviour among hatchling and juvenile reptiles is limited, due to the often

small, cryptic and secretive nature of many species during this early life stage [21].

159

For crocodilians, detailed information on agonistic behaviour is available for the

adults of three species (Crocodylus acutus, Crocodylus niloticus, and Alligator

mississippiensis; [22] [23] [24], and recently, for hatchlings and juveniles of two

species (Crocodylus porosus; Crocodylus johnstoni) [25] [26]. The results suggest

that some agonistic behaviours are shared by different species whereas others are

species-specific. However, all appear subject to species-specific variation in the way

they are expressed in different contexts and the way they change ontogenetically.

Comprehensive studies of hatchling and juvenile C. porosus and C. johnstoni under

captive conditions have recently revealed that a full repertoire of species-specific

agonistic behaviours are displayed during the first few weeks and months post-

hatching [25] [26]. For both species, clutch specific differences were observed in the

frequency and intensity of agonistic interactions, but importantly not in the range of

behaviours displayed [25] [26]. However, a wide range of other factors (eg. size, sex,

age, habitat type and complexity, density, parental care, wild vs captivity) can also

potentially influence the nature and expression of agonistic interactions, even within a

species. While this makes comparative studies difficult, detailed behavioural

observations are still informative, given the significant gap in knowledge about

agonistic behaviours for most species, for all life stages.

In this study, we observed and compared agonistic behaviour of four species of

hatchling and seven species of juvenile crocodilians representing all three crocodilian

lineages (Crocodylidae, Alligatoridae, and Gavialidae). The work was carried out in

captive conditions, because it was a practical approach that allowed control over

160

many, but not all variables.

The aims of the research were:

a. To determine whether all species engaged in agonistic interactions, and for

those that did, to describe and quantify the behaviours used to elicit and

respond to aggression.

b. To quantify inter-specific differences in types of behaviour and in the

frequency, timing, duration, intensity and outcome of an interaction, and

where possible, ontogenetic shifts in these parameters between hatchlings and

juveniles.

c. To discuss species-specific differences in agonistic behaviour among the seven

species examined and the ecological and evolutionary significance of these

differences and their relevance to conservation, management, and/or

production.

Materials and Methods

This project was conducted under the approval of the Animal Ethics Committee of

Charles Darwin University (permit no. A11003).


161

Hatchling and juvenile saltwater crocodiles (Crocodylus porosus - CPO), Australian

freshwater crocodiles (Crocodylus johnstoni - CJ), American alligators (Alligator

mississippiensis - AM), and juvenile New Guinea freshwater crocodiles (Crocodylus

novaeguineae - CNG) were provided by Wildlife Management International (WMI)

and were examined in Darwin, Australia, 27 December 2011 to 27 March 2013 (Table

1). Hatchling and juvenile Gharials (Gavialis gangeticus - GG), and juvenile Siamese

crocodiles (Crocodylus siamensis - CS), and dwarf caimans (Paleosuchus

palpebrosus - PP) were provided by the Madras Crocodile Bank Trust (MCBT) and

were examined in Chennai, India in September 2012 (Table 1).

162

Table 1. Groups of hatchling (10-21 days of age) and juvenile (10-18 months of age) crocodilians used in behavioural experiments. H:

hatchling; J: juvenile.

Species Location Date

Age

class Age

Groups

(animals)

No.

clutches TL (mm) BM (g)

Sex

ratio

A. mississippiensis

(AM) WMI 27-Mar-13 H 10-14 days 2(4) 2 234.6 ± 12.7 45.3 ± 6.9 -

WMI 27-Mar-13 J 12 months 1(4) 1 357.3 ± 7.0 118.8 ± 6.3 2M:2F

P. palpebrosus (PP) MCBT 14-Sep-12 J 12 months 3(12) 1 450.1 ± 7.9 361.4 ± 21.8 9M:3F

G. gangeticus (GG) MCBT 13-Sep-12 H 21 days 2(8) 1 504.7 ± 38.9 172.4 ± 34.6 -

MCBT 13-Sep-12 J 12 months 3(12) 2 718.5 ± 25.4 566.5 ± 76.3 8M:4F

C. porosus (CPO) WMI 16-Mar-12 H 10-14 days 3(12) 3 288.8 ± 4.9 74.2 ± 6.2 9M:3F

WMI 12-Jun-12 J 12-18 months 3(12) 3 679.6 ± 11.2 794.8 ± 38.1 10M:2F

C. johnstoni (CJ) WMI 27-Dec-11 H 10-14 days 3(12) 3 245.3 ± 5.3 42.7 ± 4.8 8M:4F

WMI 14-May-12 J 12-18 months 3(12) 3 605.4 ± 19.9 631.0 ± 67.6 9M:3F

C. novaeguineae

(CNG) WMI 18-Jan-12 J 14 months 3(12) 1 558.7 ± 15.6 491.8 ± 39.3 8M:4F

C. siamensis (CS) MCBT 11-Sep-12 J 14 months 4(16) 1 545.2 ± 13.5 475.5 ± 35.7 11M:5F

163

Each species varied in general morphology, particularly snout shape, and had different

ecological and natural history traits in the wild (Table 2). The family Alligatoridae

(AM, PP) has been separated from other extant crocodilians by 85-90 million years,

and the Gavialidae (GG) and Crocodylidae (CJ, CNG, CPO, CS), separated from

each other by 55-60 million years [27]. Snout shape categories used here are derived

from [28] which were a modification of the categories determined by [29] based on

cross-sectional dimensions and the ratio of rostral length to skull length. Several

authors have argued that snout shape in crocodilians is more closely related to

ecological habit than to phylogeny [28] [30].

164

Table 2. General characteristics of the seven species of crocodilian examined [31]. Snout shape is defined as long, generalised, or blunt

according to [28]. Species information was derived from [32] and [33].

Mean max. size

Species

Geographical

location Snout shape Primary habitat type Male Female

Nesting

strategy

Clutch

size

A. mississippiensis (AM) south eastern USA Generalised

Freshwater swamps, marshes,

and lakes 4m 3m Mound 20-50

P. palpebrosus (PP) South America Blunt

Heavily forested freshwater

rivers, creeks and flood plain 1.5m 1.2m Mound 10-20

G. gangeticus (GG) Indian subcontinent Long Freshwater rivers 5m 3.5m Hole 30-50

C. porosus (CP) south east Asia Generalised

Widespread in waterways

from coastal to far inland 5m 3m Mound 30-60

C. johnstoni (CJ) northern Australia Long

Freshwater swamps,

billabongs, rivers and creeks 3m 2m Hole 10-20

C. novaeguinea (CN)

Papua New

Guinea; Indonesia Generalised


and lakes 3.5m 2.5m Mound 20-45

C. siamensis (CS) south east Asia Generalised


and lakes 4m 3m Mound 20-50

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All animals had been raised in captivity since hatching in relatively small groups (3-

15) in enclosures of various shapes and designs containing land and water areas. Four

species involved individuals from multiple clutches (AMh, CJ, CPO, and GGj), while

all others were siblings from single clutches. Clutch differences have been reported in

the frequency and intensity of agonistic interactions [25] [26], but not in the repertoire

of behaviours displayed.

From earlier studies with CPO and CJ hatchings and juveniles it was known that

reorganizing crocodiles into small groups (3-5 individuals) increased the probability

that agonistic interactions would occur, and that the various species-specific

behaviours would be displayed, as members adjusted to their new social setting.

Hence the crocodiles here were transferred to experimental enclosures (WMI and

MCBT) in groups of 4 individuals at the same time (1200 h). Total length (TL - mm)

and body mass (g) of each animal was recorded and sex determined where possible.

Groups contained individuals of a similar size and with a similar sex ratio, which was

male biased (Table 1).

Enclosures at WMI were fibreglass and rectangular (170 x 100 x 50 cm high), with a

land area (40 %) that gradually sloped down to a water area (60 %; < 8cm deep). At

MCBT, circular plastic enclosures were used (120 x 120 x 80 cm high), with a land

area (40 %) that gradually sloped down to a water area (60 %; < 8cm deep). While the

amount of space per individual differed between both locations, our previous studies

on agonistic behaviour of hatchling and juvenile C. porosus [25] and C. johnstoni

[26], involving groups of 5 (0.34 individuals/m2) in the same enclosures used here

166

with groups of 4 (0.43 individuals/m2), revealed very similar results in terms of the

frequency, intensity, and behaviours displayed. Water temperatures were maintained

at 30-32°C (WMI) or 29-31°C (MCBT), while air temperatures varied from 26-32°C,

with a natural light cycle. These temperatures are within the range either preferred by

most crocodilians under captive conditions [34], or within the range that results in

optimal rates of growth and survival. The thermal regime that crocodilians were

exposed to prior to the study was also similar. Animals were not fed for the duration

of the observations (48 hours). No form of cover was provided which enabled clear

viewing of interactions.

Recording behaviour

Wide angle infrared CCTV cameras (Signet, 92.6º) in each enclosure recorded

behaviour on digital video recorders (Signet 4CH QV-8104). A recording period

lasted 16 hours (1600 to 0800 h), and was conducted on two consecutive nights for

each group (32 h per group). The recordings were started four hours after the

crocodiles were placed in the new experimental enclosures. This sampling period was

based on previous recordings (100’s of hours) of the hatchlings and juveniles of

several species (CPO, CJ, CNG, GG, CS, AM) that revealed no agonistic behaviour

occurring between 0800 and 1600 h. For all these species, agonistic interactions

corresponded with periods of increased activity, mostly occurring at dusk and early

evening (1600-2200h). No audio was recorded during this study, but some species did

vocalize. Vocalization produced distinctive ripples in the water, which were visible on

the film, allowing some but not all vocalizations to be detected.

167



aggression and intolerance appeared to be signalled by postures or actions by one or

both individuals [25] [26]. An aggressive individual was one that made deliberate

advances toward another, or that made physical contact with another. Each agonistic


aggression. The intensity of agonistic interactions was characterised as: low or high.

Low intensity interactions appeared accidental, when individuals lying together

disturbed each other when moving, or if one swam into another underwater. High

intensity interactions appeared deliberate, with one individual approaching another

with the apparent goal of initiating an agonistic interaction. The behaviour exhibited,

the intensity of interaction (low or high), the location (water, land), the time, duration

of interaction and outcome (displacement or no displacement) were all quantified, as

previously described for hatchling CPO and CJ under similar conditions [25] [26].

Classification of behaviour


inventory of agonistic behaviour, similar to that described for hatchling and juvenile

CPO and CJ [25] [26]. The descriptions are based on a series of basic postures,

modified by movement of body parts or of the whole animal, and whether visual

signals or actual contact was involved [25] [26]. Some of these behaviours have been

168

described in other studies with juvenile and adult crocodilians [22] [18] [25] [26].


All statistical analyses were performed using JMP 8.0 statistical software [35]. Where

appropriate, data were checked for normality (Shapiro-Wilk’s test) and

homoscedasticity (Cochran’s test) prior to statistical analysis. Due to the potential

influence of clutch on the frequency, intensity, duration, and outcome of agonistic

interactions, statistical analyses were limited to species with more than one clutch

(AMh, CJ, CPO, GGj). However, the data is still presented for other species because

there are so few data of this sort in the literature. Frequency and duration of

interactions was compared among species using a Kruskal-Wallis test with Wilcoxon

pair-wise comparisons to account for small and unequal sample sizes. A Pearson’s

chi-square test was used to compare the intensity and outcome of an interaction

among species. Hatchlings and juveniles were compared separately in all species. A

significance level of P<0.05 was used for all statistical tests. All means are reported ±

one standard error with sample sizes.

Results

Agonistic behaviour

In 960 h of observation of 120 individuals of seven species, we observed a total of

462 agonistic interactions. Observed agonistic interactions occurred in open water,

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with none observed on land. All interactions involved only two animals, with the

single exception of three juvenile. For most species, interactions appeared to occur

accidentally when individuals lying together disturbed each other when moving off, or

if one swam into another. However, interactions were also initiated by one individual

moving deliberately toward another in either a single movement or in a series of short,

rapid advance (RA) movements. In response to an approach, an animal displayed a

series of other agonistic behaviours (Table 3).

Table 3. Description of the various postures, non-contact and contact movements

displayed by hatchling and juvenile crocodilians during agonistic interactions

[30] [31]. *= has not been previously described, or is different in some way.


Initiation

Rapid advance RA

Series of short rapid advance movements towards another

individual while low in water

Termination

Slow flight SF

Slow movement away from another individual in a low in

water posture.

Rapid flight RF

Rapid movement away from another individual in a low in

water posture.

Posture

Low in water LIW

Immobile with only the top of the head and back above the

water surface.

Inflated posture IP

Immobile with upward extension of either the front two or all

four limbs, with neck and back arched high and head and tail

angled downward.

Head and tail

raised HTR

Immobile with head and tail raised out of water while back

remains low. Head is usually parallel to the water but can also

be angled upwards.

Head raised high HRH

Immobile with upward extension of the front two limbs

pushing the head and chest high out of the water on a ~45º

angle while tail remains low.

Mouth agape MA Immobile with mouth opened wide (all postures).

Non-contact movements

Light jaw-clap LJC

Rapid opening and closing of the jaws at the water surface,

often repeated several times while low in the water or inflated.

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Tail-wagging TW

Undulation of the tail from side to side in either a gentle

sweeping motion or rapid twitching, often repeated several

times (all postures).

Inflated tail sweep ITS*

In an inflated posture, the whole tail is swept side to side in a

slow deliberate fashion as the individual approaches another.

This becomes more rapid and the tail is thrashed from side to

side.

Vocalization V* Vocalization observed and confirmed from body movement.

Contact movement

Head push HP

Head is pushed in to an opponent, usually with mouth closed

while low in water or inflated.

Push down PD

Chest and neck of individual pushed down on the upper neck

or back of an opponent while head is raised high.


Side head-strike SHS

Head is thrust sideways in to an opponent while the mouth is

either open or closed (all postures).

Tail-wag side

head strike TWSHS

Tail wagging occurs prior to a side head strike, increasing the

force of the impact (all postures).

Tail-wag bite TWB

Tail wagging occurs prior to a bite and it propels the individual

in to an opponent with force while low in water.

Agonistic behaviours involved the adoption of some discrete postures that varied in

the intensity of expression (Table 3). The adoption of such postures could be

abandoned at any time by either slow (SF) or rapid flight (RF), ending the interaction.

Alternatively, the signals emanating from the postures could be intensified with body

movements, such as mouth agape (MA), light jaw claps (LJC), or tail wagging (TW),

which were signalling displays that did not involve physical contact between

combatants. If the agonistic interaction was not terminated by flight (SF or RF) by one

or both animals, the behaviours intensified, with contact movements such as head

pushing (HP), push downs (PD), biting (B), or side head striking (SHS), occasionally

combined in different ways with intense tail wagging (Table 3), until one or both

individuals took flight. While several behaviours were common across the majority of

species, other behaviours were often specific to only one or a couple of species, varied

in the frequency with which it was exhibited (common or rare), and in some cases

appeared to be used to signal different intentions (Table 4).

171

When not involved in agonistic interactions, individuals of most species would lie

close together in the water. CS was observed rubbing the sides of their snouts against

each other while lying together in what appeared to be some form of non-aggressive

communication. In contrast, close contact rarely occurred among juvenile CPO, CNG

and PP, which tended to separate from each other.

172

Table 4. Presence or absence of the various postures, non-contact and contact

movements displayed by hatchling (H) and juvenile (J) crocodilians during

agonistic interactions [25] [26]. AM: A. mississippiensis, PP: P. palpebrosus, GG:

G. gangeticus, CPO: C. porosus, CJ: C. johnstoni, CNG: C. novaeguineae, CS: C.

siamensis.

Species

AM PP GG CPO CJ CNG CS

Initiation H J J H J H J H J J J

Rapid advance (RA) X X X X X

Termination

Slow flight (SF) X X X X X X X X

Rapid flight (RF) X X X X

Posture

Low in water (LIW) X X X X X X X X X X X

Inflated posture (IP) X X X

Head and tail raised (HTR) X

Head raised high (HRH) X X X X X X X

Mouth agape (MA) X X X X X X X X


Light jaw-clap (LJC) X X X

Tail-wagging (TW) X X X X X X

Inflated tail sweep (ITS) X

Contact movement

Head push (HP) X X X X X X X X X X X

Push down (PD) X X

Bite (B) X X X X X X X X X X

Side head-strike (SHS) X X X X X

Tail-wag side head strike

(TWSHS) X X

Tail-wag bite (TWB) X X X X X X

Postures

Crocodilians of all species and ages most commonly remained low in the water (LIW)

during an agonistic interaction and while at rest (Table 4; Fig. 1). However, GG and

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CJ adopted postures with their heads raised ~40º to the body, while PP lay with its

head raised up but parallel to the water surface (Fig. 1). In most cases, remaining LIW

did not signal aggressive intent, unless used by aggressive individuals during an

approach, which was commonly observed among juvenile CPO, CNG, and PP.

Figure 1. Agonistic behaviours displayed by young crocodilians. Postures, non-

contact and contact movements (described in Table 3) displayed by hatchling (h) and

juvenile (j) crocodilians. Crocodilians in the figure include G. gangeticus - h (a); P.

palpebrosus (b); C. siamensis; (c); C. porosus - h (d,e,f,g,h); C. novaeguineae (i); C.

johnstoni - j (j); C. porosus - h (k,l).

The head raised high (HRH: ~45º) posture was observed in five species (CJ, CNG,

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CPO, GG, PP; Table 4) where it appeared to signal aggressive intent, submission or

avoidance. In juvenile CNG and CPO, HRH clearly signalled submission, while in PP

and hatchling CPO it signalled readiness to give or receive contact. In CJ and GG,

HRH generally signalled avoidance and was more common among juvenile than

hatchling CJ.

The inflated posture (IP) was only observed in two species (CNG, CPO; Table 4) and

in CNG was a common and clear display of aggressive intent. The head and tail raised

(HTR) posture was only observed in hatchling CPO (Table 4) and while rarely

displayed, signalled aggressive intent. Mouth agape (MA) was observed in all but

three species (hatchling AM and CJ; juvenile CS; Table 4) and was displayed by

aggressive individuals as a threat or by submissive individuals when approached by

an attacker. While hatchling CPO utilised a wide range of postures, juvenile CPO

most commonly assumed a LIW posture if aggressive, non-aggressive individuals

were either in a LIW or HRH posture that signalled submission.


Light jaw claps (LJC) were only observed in CPO and CJ (Table 4), and clearly

signalled aggressive intent in hatchlings, and were absent (CJ) or rare (CPO) in

juveniles. Tail wagging (TW) signalled high agitation and was displayed by

aggressive individuals as forewarning of a contact movement, and by non-aggressive

individuals in anticipation of an attack by an approaching individual. Tail wagging

often increased in intensity as an interaction escalated. Inflated tail sweeping (ITS)

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was only observed in CNG and was a highly aggressive non-contact movement that

increased in intensity as an interaction escalated (Fig. 1). It differed from TW in that

the whole tail was involved, sweeping from side to side.

Vocalizations that created ripples in the water were observed in juvenile CS, CNG,

and hatchling and juvenile AM. In CS and AM, vocalizations did not appear to be

associated with aggression. While the initial reason for vocalizing was often unclear,

if one individual vocalized between 1 and 3 of the others often responded. On one

occasion, a juvenile AM vocalization resulted in the other three individuals swimming

over from their place of rest towards the vocalizing individual. Then all four AM

juveniles initiated foraging behaviour. In contrast, vocalizations by CNG occasionally

preceded the initiation of an agonistic interaction.

Contact movements

Contact was made during the majority of agonistic interactions (88-100%) in all but

juvenile CPO (42.2%), hatchling and juvenile GG (H=20%; J=36%), and juvenile PP

(45.7%). For juvenile CPO, PP, and CNG (70.7%), an attempt at contact was usually

made, but the individual under attack often took flight (RF, SF) and avoided actual

contact. In contrast, in hatchling and juvenile GG contact was rarely even attempted.

Head pushes (HP) and bites (B) were the most common form of contact used by all

species of crocodilian. HP was the least aggressive form of contact, usually directed at

the body. Bites were mostly directed at the head or body or at the tail if an animal fled

176

(common in CPO and CNG). AM commonly grabbed hold of another individuals’

snout, while bites by CS, GG and CJ juveniles were only very light. In general, GG

and CJ juveniles avoided physical contact involving the head. Push downs (PD) were

low intensity and only observed in CJ, more frequently among juveniles than

hatchlings (Fig. 1). Side head strikes (SHS) and SHS and bites accompanied by tail

wagging (TWB) were a highly aggressive form of contact displayed by only a few

species [(SHS: CNG, PP, CJ(h), CPO (h,j); TWB: CNG, CS, CPO (h,j); Table 4].

Side head strikes accompanied by tail wagging (TWSHS) were another highly

aggressive form of contact only observed in CPO hatchlings and juveniles (Fig. 1).

While hatchling CPO displayed a range of contact movements, juveniles mostly

displayed TWBs.


Aggression

An aggressive individual was defined as any individual that made deliberate advances

toward another and, or which made deliberate physical contact with another [30] [31].

Each agonistic interaction was examined to quantify whether one or both contestants

engaged in aggression, and whether this differed among species. For most species,

only one individual appeared aggressive during an agonistic interaction. However,

both individuals appeared aggressive during interactions between hatchling (51.9%)

but not juvenile CPO (0%), in both hatchling (27.8%) and juvenile (35.7%) CJ, and in

a few of interactions between juvenile CNG (8.6%).

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Frequency and duration

Agonistic interactions for most species occurred sporadically throughout the night and

early morning with the majority between 1600-2200h. However, in CPO there was a

more defined pattern, with the majority occurring predominantly at dusk (1700-

1900h) and dawn (0600-0800h). The mean number of agonistic interactions (X2 =

30.80, df = 5, P < 0.05) and mean duration of interactions (X2 = 142.88, df = 5, P <

0.05) observed per group per night among the four species from multiple clutches

varied significantly (Table 5). The frequency and duration of agonistic interactions

was highest for CPO juveniles and hatchlings, while the frequency of agonistic

interactions was lower in juvenile CJ compared with hatchling CJ (>2 times), and was

highest among juvenile CPO compared with hatchlings (>2 times).

188

Table 5. The frequency, duration, intensity, and outcome of agonistic interactions between young crocodilians. Different letters indicate

significant difference.

Species Age

class

No.

interactions

Frequency

per night

Mean

duration

Intensity

(%high)

Outcome

(% displacement)

Multiple clutches

C. porosus J 147 24.7 + 3.53A

19.1 + 0.77B

95.9A

100A

C. porosus H 52 8.7 + 0.88B

49.3 + 4.89A

75B

63.5B

C. johnstoni H 36 6.0 + 0.63B,C

13.4 + 1.30B,C

38.9C

30.6C

C. johnstoni J 13 2.3 + 0.21C

13.0 + 2.44B,C

30.8D

38.5C

A. mississippiensis H 24 4.2 + 0.31C

8.5 + 0.57C

0E

0D

G. gangeticus J 25 4.2 +0.60C

5.6 + 0.21C

0E

36C

Single clutches

C. novaeguineae J 56 9.3 + 0.71 18.6 + 1.88 67.9 60.7

P. palpebrosus J 32 5.3 + 0.42 8.9 + 0.82 55.2 43.8

C. siamensis J 64 8.1 +0.67 6.05 + 0.25 7.8 9.4

A. mississippiensis J 8 4.0 + 0.0 9.3 + 1.03 12.5 0

G. gangeticus H 5 1.3 + 0.5 3.6 + 0.40 0 0

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The duration of agonistic interactions was longer among hatchling CPO compared

with juveniles, but was similar between juvenile and hatchling CJ. Between juvenile

CS and hatchling AM, two individuals grabbed each other and did not let go for an

extended period (CS: 484 s; AM: 42 s) in which they rolled around together. In the

only interaction to involve more than two individuals, three juvenile CJ came together

with their snouts raised up high and then began a series of PDs while biting. As they

did this, they moved in a circular motion and this continued for 51 seconds.

Intensity and outcome

The intensity of interactions differed among the four species with multiple clutches

(X2 = 176.27, df = 5, P < 0.05; Table 5). The frequency of high-intensity interactions

was highest for hatchling and juvenile CPO, followed by hatchling and juvenile CJ.

None of the interactions between hatchling AM and juvenile GG were high intensity.

The instigator was usually the winner of interactions between juvenile CPO (100%),

but for most species it was generally unclear whether either individual had won (0-

36%) due to the predominance of low intensity interactions. The outcome of

interactions differed among species from multiple clutches (X2 = 163.55, df = 5, P <

0.05; Table 5). In contrast to the other species (hatchling and juveniles), the majority

of interactions between juvenile CPO resulted in the loser being displaced.

190

Discussion

Agonistic behaviour

Many of the behaviours observed during agonistic interactions among juvenile

crocodilians in this study have also been reported among adults [22] [18] [24], which

suggests that agonistic behaviour, as with other behaviours in crocodilians [19], may

be hard wired from birth and stereotypical for most species. However, for a particular

species, certain behaviours may be present or absent at different life stages, or only

used when the prevailing social context requires. However, behaviours shared by

different species often varied in frequency and intensity (eg. tail wagging) and could

be used to signal different intentions (eg. head raised high).

Of the behaviours displayed by juveniles in this study, three were common to all

seven species (Low in water; head push; bite), and three were specific to only one

species (Push down: CJ; Inflated tail sweeping: CNG; Tail wag side head strike:

CPO), while the other behaviours were displayed by some and not others (Table 4).

Of the behaviours displayed by hatchlings in this study, two were common to all four

species (low in water; head push). Five were shared by CJ and CPO hatchlings (RA,

TWB, SHS, LJC, TW). Four behaviours were unique to CPO (RF, IP, HTR,

TWSHS), and one to CJ (PD) (Table 4). Among hatchlings compared, only AM

hatchlings were observed to vocalize.

Individuals of most species remained low in the water during agonistic interactions

191

that did not signal aggressive intent, while inflating the body or raising the head and

tail combined with mouth agape was a clear sign of aggression. However, among

species with a more defined pattern of dominance (CPO, CNG) aggressive individuals

would remain low in the water when approaching a subordinate. The head raised high

posture was most commonly used to signal submission, while tail wagging indicated

high agitation.

Inflating the body and opening the mouth to signal aggressive intent and raising the

head high to indicate submission are postures used by several species of sub-adult and

adult crocodilian [22] [18]. Many species of birds [36], mammals [1] [2], and fish [37]

[38] will also raise or inflate their body and open their mouth wide during agonistic

interactions in an attempt to intimidate their opponent.

In most cases, this type of display enables both individuals to assess the potential

combative ability of the other and is often sufficient to prevent physical contact

through causing one individual to retreat [39] [40]. The use of tail wagging to signal

high agitation has also been observed in sub-adult and adult crocodilians [22], along

with certain species of lizards [41], mice [42] and salamanders [9].

The main forms of contact during interactions for most species in this study were head

pushes and bites. Bites could range in severity from light mouthing (CS) or grabbing

and letting go, which were most common, to bites in which the aggressor either

propelled itself into another individual, or bites in which the individual grabbed and

shook before letting go. On the extreme end of the scale, a few interactions between

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individuals from less aggressive species (CJ, AM, CS) resulted in two individuals

grabbing each other and rolling around with neither letting go for an extended period.

Biting is the most common form of contact used during agonistic interactions in other

reptiles [43], birds [3], mammals [1] [2], and fish [44] [45].

There were essentially three agonistic behaviours observed that appeared to be

specific to only one species: push down by CJ; inflated tail sweep by CNG; and, the

side head strike combined with tail wagging by CPO. The push down by CJ may have

evolved in response to its elongated snout that is presumably more vulnerable to

damage by contact such as bites or side head strikes. The inflated tail sweeping by

aggressive CNG provided subordinates with a clear warning of aggressive intent,

giving them time to take flight and avoid an attack. A similar behaviour has also been

observed in skinks, and is described as ‘tail lashing’, which precedes biting and

chasing [41] [46].

Tail wag side head striking by CPO was the most aggressive contact movement

observed in any species of crocodilian, and is similar to that observed between rival

adult male CPO during the breeding season [47]. While infrequent, tail wag side head

striking was more common among hatchlings and occurred when both individuals

were aggressive. One or both individuals would typically align head to head and raise

themselves up with the head raised high, before swinging the head violently into the

head or body of the other individual. The object of this contact movement appeared to

be to inflict maximum damage and may be an important behaviour, along with tail

wag biting, in establishing dominance in this species.

193

Most animals avoid the use of severe or injurious forms of contact during interactions,

unless the stakes are high enough to justify the risk, such as during the acquisition of

mates, food, shelter or territory [48]. However, the use of such intense agonistic

behaviours may also be important in establishing dominance, as the loser of these

interactions may be less likely to challenge again in the future and become

subordinate [13]. Many species typically engage in intense forms of agonistic

interactions involving more highly aggressive behaviours during the juvenile stage

until a dominance hierarchy is formed [49] [13].

In terms of snout morphology, crocodilians have been broadly categorised as blunt-

snouted, generalised, or long-snouted, [28], in which the potential for the snout to be

damaged during interactions increases respectively [50]. In this study, two

crocodilians were long-snouted (GG and CJ), four were generalised (AM, CPO, CS,

CNG) and one was blunt-snouted (PP). During agonistic interactions the two long-

snouted species (CJ, GG) raised the head and generally avoided contact involving the

head, while the generalised and blunt-snouted species often made contact with the

head. Species of salamander that have morphologically more vulnerable head shapes

are also known to employ less injurious forms of contact than those with more robust

shapes [9].

Non-aggressive behaviour

Several behaviours were observed that were not involved in agonistic interactions.

194

Juvenile CS would often lie close together in the water, and were often observed

rubbing the sides of their snouts together. This behaviour was not associated with

aggression and appeared to be some form of social recognition or communication

which has also been observed among males and females during the breeding season

[51] [52]. In crocodilians, the side of the snout contain numerous integumentary

sensory organs that are highly sensitive to external stimuli [18] [53] [54], and may

play an important role in communication. Chemoreception in crocodilians is also

acute, and has been implicated in behavioural responses of juveniles and adults to skin

gland secretions [55] [56].

While the majority of species remained low in the water while at rest, CJ, GG, and PP

lie with their heads raised up on an angle. However, while CJ and GG angled their

head up high, the head of PP remained parallel to the water in a ‘dog-like’ pose

commonly observed in caiman species. While the significance of these raised postures

remains unclear, it is possible that they have evolved in response to a need to keep

vigilant for predators, including larger crocodiles, given that these species either

remain quite small (CJ, PP) for an extended period of time, or are physically more

vulnerable (CJ and GG).

Vocalizations of sufficient intensity to ripple the water were made by juvenile CS and

CNG, and by hatchling and juvenile AM. For CS and AM, they did not appear to

signal aggression but did result in a response from other individuals. For CS and AM,

the other individuals often responded by vocalizing themselves, while on one

occasion a series of vocalizations by one AM resulted in the commencement of

195

foraging behaviour by three pen mates. In contrast, vocalizations by CNG did appear

to be linked to aggression, and were observed on one occasion preceding an

aggressive advance, and on another occasion resulting in a nearby subordinate taking

flight rapidly.

Vocal communication has been widely reported among crocodilians, especially during

the hatchling stage when crèches are maintained, and among adults during the

breeding season [24] [57]. As we did not record sound during these experiments it is

likely that vocalizations were more common than reported here. Nevertheless, the

three species observed vocalising here are all known to occupy densely vegetated

habitats such as freshwater swamps and lagoons, where vocalization may play a larger

role in communication than with species that live mainly in open water areas [18]

[58]. Previous studies have suggested that juvenile vocalizations serve two primary

functions: (1) contact calls localize individuals and facilitate grouping, and (2) distress

calls signal potential predators and promote defence by larger individuals [59] [60].

Vocalizations related to aggression in young crocodilians have not previously been

reported, and would constitute a possible third, and new, functional category of

juvenile vocalizations.

Aggression and dominance

The large majority of interactions among the less aggressive species of juvenile

crocodilian appeared accidental. Despite a similar or higher frequency of agonistic

interactions between CS compared with CNG and PP, interactions were generally low

196

intensity with individuals often observed lying together. While biting occurred during

interactions, it was mostly light mouthing.

Agonistic interactions between juvenile CJ, AM, and GG were infrequent and

considered very low level with individuals highly tolerant of others. The frequency of

agonistic interactions in AM and GG were similar in hatchlings and juveniles, while

the frequency of agonistic interactions between hatchling CJ was almost twice that of

juveniles, although in both age classes there was limited contact with the head and a

high frequency of push downs on their opponent.

Behaviour suggesting dominance hierarchies was observed among juvenile CPO,

CNG, and to a lesser extent PP. Agonistic interactions among these species were

characterised by an aggressive individual advancing towards another, either low in the

water (CPO, PP, CNG) or while inflated and tail thrashing (CNG), and the

subordinate individual responding by remaining low in the water or rising with the

head raised high before taking flight. In CPO and CNG, the aggressor often gave

chase and attempted to bite or tail wag bite, while PP struck sideways with the head.

However, with CPO, these behaviours were most obvious in juveniles rather than

hatchlings.

Dominance hierarchies appear common in crocodilians in the wild and in captivity

[18], and the formidable morphological armour crocodilians are endowed with could

be important for preventing serious injury or death during agonistic interactions linked

to establishing dominance [48]. The nature and extent of dominance varies across

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species [18] and appeared to be correlated with the general level of aggressive

behaviour in adults.

While the formation of a dominance hierarchy may be more rapid under captive

conditions, the results of this study demonstrate that dominance and agonistic

behaviour develops early in highly aggressive species of crocodilian, and may

ultimately be a strategy for the early honing of avoidance skills that minimise the

potential for injury. In contrast, dominance appeared less important among the other

five species, which displayed low levels of aggression and a higher tolerance of

conspecifics at this early life stage. These less aggressive species also displayed fewer

types of behaviours than the more aggressive ones. This absence or loss of behaviours

has previously been reported in other animals in which dominance is considered less

important [14].

Hatchlings of almost all crocodilian species studied to date will form tight-knit

crèches in the immediate post-hatching period before dispersing anywhere from a few

days to several years later. While information on crèche formation and dispersal is

lacking for most species of crocodilian, it may help explain the species-specific

variation in agonistic behaviour and social tolerance between hatchlings and juveniles

in certain species. For AM and CS (low aggression), hatchlings within swamp or

marsh habitats are known to remain together accompanied by the female and older or

younger siblings for up to several years [18] [61]. Hatchling GG (low aggression)

from multiple clutches form large creches of 100-1000 individuals which remain

together for 2+ months, typically accompanied by adult females and a defensive male

198

[62].

In contrast, hatchling CPO (high aggression) remain together in crèches anywhere

from one week up to two months at which point dispersal is considered to occur due

to a growing intolerance of each other [63]. However, hatchling PP, that were

considered relatively aggressive in this study, were recently found to crèche together

in small groups accompanied by a female up to 12 months post-hatching [64]. During

this time, the size of the crèche steadily decreased, which could be due to mortality

(eg. predation) or a growing intolerance of each other. The relatively high level of

aggression among 12 month old PP in this study would suggest that agonistic

behaviour may at least play a role in dispersal.

While adult crocodilians are often less tolerant of conspecifics than hatchlings or

juveniles, insome species, large numbers of adults group together in large numbers at

different times throughout the year [18]. Among the less aggressive species in this

study, CJ, CS, and AM are all known to congregate together seasonally in large

numbers due to lower water levels in the dry season [18] [65], while CJ, GG, and AM

are also known to congregate together during the breeding and nesting season [18]. In

comparison, CPO and PP have rarely been observed together at any time of the year

outside of the breeding season when they form only male-female pairs [32] [33].

Suspension or reduction in agonistic behaviour may itself be an important strategy

enabling certain species of crocodilian to coexist in high numbers without sustaining

serious injuries [18]. That high density of conspecifics can reduce levels of aggression

has been found in certain species of trout [37].

199

Interspecific aggression

In areas where species of crocodilian exist in sympatry, there may be a competitive

advantage to being the more aggressive species, as this may result in greater access to

resources. However, while some studies of crayfish have found that the level of

intraspecific aggressiveness observed in the laboratory is often consistent with the

competitive ability of species in the wild [66] [67], others have found the opposite

[15].

In crocodilians, the nature and extent of agonistic behaviour among sympatric species

is poorly known. A recent study that examined interspecific aggression between

juvenile CPO and CJ under laboratory conditions found that despite the higher level

of aggressiveness observed during intraspecific interactions between CPO, CPO did

not dominate CJ in any way [25] [26]. Instead, dominance appeared to be related to

body size, with smaller individuals avoiding larger ones regardless of species.

Agonistic interactions were only observed between similar sized individuals of both

species, with no clear winner in the interactions observed due to the different

strategies employed. Hence the much larger size that adult CPO attains relative to

adult CJ may give it the competitive ability, forcing CJ to adapt and evolve

morphologically, behaviourally and ecologically. Larger body size rather than

intraspecific aggression is also a greater determinant of competitive ability among

several species of crayfish [68] [69], and fish [37].

200

Species comparisons

Based on our studies of four species at WMI, we are able to construct a relative

ranking of high to low aggression of CPO>CNG>CJ>AM. The relative ranking of the

species studied at MCBT on the same scale is PP>CS>GG. If we then collate our

findings at WMI with three additional species at MCBT, the relative ranking on a high

to low aggression scale for the seven species studied is:

CPO>CNG>PP>CS>CJ>AM>GG. Although we only focused on hatchlings and

juveniles of seven species in this study, the relative ranking of these seven species

provides new information that can be integrated with other more recent data into an

updated version of Lang’s [18] original scaling of species according to high to low

aggression and its reciprocal, tolerance vs. intolerance of conspecifics (Fig. 2). This

remains a subjective assessment, because genetics, sex, age and the environment

(captive vs wild) may all be implicated, but nevertheless updating it with additional

qualitative and quantitative new information is useful. Based on the results of our

observations reported here, we propose that slender snouted species may be far more

tolerant of each other, or at least avoid agonistic interactions involving more

damaging behaviours.

201

Figure 2. Tolerance of conspecifics in crocodilian species – updated assessment

[18]. Tolerance of conspecifics (low-high) and level of aggression (high-low) in

crocodilian species based largely on behavioural observations of social interactions

between adults and juveniles in captivity and in the wild. Information has been

sourced from published and unpublished reports, papers, theses and anecdotal

accounts. Boxes highlight species involved in this study; ? indicates minimal

information; arrows indicate direction of update.

The most significant changes are that CS, originally considered a fairly aggressive

species with a low tolerance of conspecifics, may not be so. Adults have recently been

reported as sharing burrows in the wild [70], while another study reported animals of

different ages and sizes existing in close proximity within a lake environment [61]. In

areas where CS and CPO are farmed, CS is usually the favoured species despite its

less valuable skin [71], because the greater tolerance of conspecifics is more amenable

to captive raising. We also consider GG to be far more tolerant than first thought,

202

based on the results of this study and that juveniles and sub-adults of various sizes

have been observed together in captivity without any agonistic behaviour, injuries or

voluntary spatial segregation (M. Brien pers. observation).

C. mindorensis was not originally involved in Lang’s [18] original comparison, but is

considered by many as one of the most aggressive species of crocodilian, which has

led to difficulties in breeding this species in captivity [72]. Intraspecific aggression

among juveniles and sub adults is also reportedly high in the wild and in captivity

[72]. While C. rhombifer was originally considered less aggressive and tolerant, more

recent reports from captivity suggest that C. rhombifer may be far more aggressive

[73] and they are even known to dominate larger crocodilian species [74]. Based on

the results of this study and on observations by one of the authors (JL), we also

consider that CNG is also far more aggressive than originally thought.

Phylogenetic relationships, based on recent analyses using morphological and

molecular features, do not provide robust explanations for the differences we

observed in agonistic behaviours of young in the seven species we examined,

representing the three major lineages. A close examination of the groupings in Figure

2 indicates that representatives of the Alligatoridae (PP,AM) and of the Crocodylidae

(CPO, CNG, CS, CJ) span the continuum from high to low aggression, and

intolerance to tolerance of conspecifics. The seemingly larger suite of behaviours

documented in CPO and CJ, relative to the other species studied here (Table 4) likely

reflects the detailed investigations focused on ontogenetic changes, and the many

variables influencing the full expression of the species-specific behavioural

203

repertoires [25] [26].

Conclusions

Variation in the nature and extent of agonistic behaviour in crocodilians may reflect

evolutionary divergence associated with differences in morphology, ecology, and

general life history. In areas where more than one species exists, this divergence may

have even been shaped by the more dominant species of crocodilian. Understanding

interspecific differences in the level of aggression and social tolerance has

implications for conservation and management programs that involve captive

breeding and reintroduction. For example, how aggressive a species is towards

conspecifics at a particular life stage will influence not only how they are raised in

captivity but also how reintroductions need to be undertaken to be successful. In areas

where more than one species coexists, either naturally or through artificial

introductions, an understanding of interspecific aggression can also be used to assess

the competitive ability of each species and the potential of an invasive species to

displace a native one.

This study indicates that many behaviours displayed by crocodilians are evident early

in life, and that hatchlings do exhibit a wide range of behaviours that may change or

disappear with age, but are similar to the behavioural repertoires known to

characterize adults. Although the seven species studied here included representatives

of the three major crocodilian lineages alive today, the New World caiman species are

underrepresented, as well as species of New World crocodiles, and the other

204

representative of Gavialidae, the genus Tomistoma. Cataloguing the behavioural

repertoires of young in these unstudied species will be of value in advancing species

comparisons.

The diverse and complex nature of crocodilian behaviour and communication is

similar to that observed in birds and mammals [18] [19]. In this study we focussed on

visual displays of hatchlings and juveniles during agonistic interactions. However,

crocodilians are also capable of vocal and chemical communication, which will likely

be productive for further studies. Future research on agonistic behaviour in

crocodilians should focus not only on the visual components, but also the role of

vocalizations and chemical cues, and how these may develop with age. Future

research will also be important for determining whether species-specific behaviours

reported here are in fact consistent for the species as a whole, and whether this may

differ in the wild.

Acknowledgements

We thank Charlie Manolis, Jemeema Brien, Elize Dorrestein from WMI for their help

in different phases of the project; Toody from Melanesia (Green Island, QLD) for the

supply of C. novaeguineae; Tim Faulkner, Julie Mendozona, and staff at the

Australian Reptile Park (Gosford, NSW) for help and supply of A. mississippiensis;

and Rom Whitaker, Gowri Mallapur, Nikhil Whitaker, Gayathri Selvaraj, and Josh

Van Lier from Madras Crocodile Bank (Chennai, India) for use of crocodilians and

facilities and general help and support. We would also like to thank Wildlife

205

Management International for the supply of animals, use of facilities and logistical

support.

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Chapter 4. Thermal preferences of hatchling saltwater crocodiles

(Crocodylus porosus) in response to time of day, social aggregation

and feeding

Published as: ‘Brien, M.L., Webb, G.J., Gienger, C.M., Lang, J.W., Christian, K.A.,

2012. Thermal preferences of hatchling saltwater crocodiles (Crocodylus porosus) in


37, 625–630’. Formatted according to author guidelines of journal.

Abstract

Three month old hatchling C. porosus with data loggers in their stomachs were placed

in thermal gradients, in isolation (N=16) and in groups of 4 (N=8 groups; 32

individuals). Mean Tb and variation in Tb (SD) was not different whether individual

crocodiles in isolation were fasted or fed, or if individuals were housed in isolation (I)

or in groups (G). However, individuals in isolation (N=16) maintained slightly lower

Tbs than those in groups (N=32) during the early morning (0600-1100h). The overall

mean Tb recorded for fasted individuals in the isolated and group treatments (N=48)

was 30.9 ± 2.3 ºC SD, with 50% of Tbs (Tset) between 29.4 ºC and 32.6 ºC, and a

voluntary maximum and minimum of 37.6 ºC and 23.2 ºC respectively. During the

day (1100-1700h), individuals in isolation and in groups selected the warmer parts of

the gradient on land, where they moved little. Outside of this quiescent period (QP),

activity levels were much higher and they used the water more. There was a strong

diurnal cycle for fasted individuals in isolation and in groups, with Tb during the QP

(31.9 ± 2.09ºC; N=48) significantly higher than during the non-quiescent period

218

(NQP: 30.6 ± 2.31ºC). Thermal variation (SD) in Tb was relatively stable throughout

the day, with the highest variation at around dusk and early evening (1800-2000h),

which coincided with a period of highest activity. The diurnal activity cycle appears

innate, and may reflect the need to engage in feeding activity at the water’s edge in

the early evening, despite ambient temperatures being cooler, with reduced activity

and basking during the day. If so, preferred Tb may be more accurately defined as the

mean Tb during the QP rather than the NQP. Implications for the thermal environment

best suited for captive C. porosus hatchlings are discussed.

Key words: Thermal preference; diurnal cycle; feeding; social aggregation;

Crocodylus porosus

1. Introduction

Many ectotherms maintain body temperatures (Tb) within a preferred range through

behavioral means, namely shuttling between warm and cool parts of their

microhabitat (Heath, 1970; Heatwole, 1977; Seebacher, 1999; Tattersall et al., 2006).

The preferred Tb range can vary throughout the day due to endogenous circadian

rhythms (Ellis et al., 2006), but it is also subject to variation by stochastic

environmental events (changed availability of warm and cool sites), the physiological

state of an individual, the social landscape in which it exists, the extent of nocturnal

versus diurnal activity, and various other factors (Heatwole et al., 1975, Huey, 1982;

Lang, 1987; Yang et al., 2008).

219

Feeding is often followed by the selection of elevated Tbs (Blouin-Demers and

Weatherhead, 2001; Gatten, 1974; Slip and Shine, 1988), but it can also be associated

with reduced or stable Tbs (Brown and Brooks, 1991; Brown and Weatherhead, 2000;

Knight et al., 1990). The response to feeding may depend on whether feeding is

nocturnal or diurnal, or the Tb experienced during feeding versus the optimal Tb for

digestive processes (Huey, 1982). Effects of feeding on Tb vary in species with highly

seasonal influences on food intake (Webb et al., 1982), and in species in which

juveniles eat small amounts of food regularly (Webb et al., 1991), versus larger adults

with a boom and bust feeding cycle and empty stomachs most of the time (Cott,

1961).

Crocodilians use both the land (sun, shade) and water (warm, cool) to regulate their Tb

(Grigg and Seebacher, 2000; Lang, 1987). As predicted by Spotila et al. (1972),

hatchlings and juveniles maintain Tbs within a narrower range than adults, which

spend relatively more time either heating or cooling their larger body mass (Grigg and

Seebacher, 2000; Lang, 1987). However, social interchange between individuals can

also interfere with, and take precedence over, behaviors aimed specifically at fulfilling

thermoregulatory needs in highly territorial species (Dewitt, 1967; Grigg and

Seebacher, 2000; Khan et al., 2010; Lang, 1987), and social status may itself co-vary

with body size and feeding strategy. The Tbs (mean and variation) that individual

crocodilians maintain in a particular thermal, social and ecological context can be

inherently complex.

The importance of thermoregulation is well recognised in crocodile farming contexts

220

(Hutton and Webb, 1992), where providing an ‘adequate’ thermal environment is

critical to survival, growth and well-being. However, studies of thermoregulation in

hatchling saltwater crocodiles (Crocodylus porosus) have been limited (Lang, 1981).

American alligators (Alligator mississippiensis) exist in climates limited by short

warm seasons, and maintaining them in captivity with high and constant temperatures

(31-32 ºC) improves health and growth rates (Joanen and McNease, 1976). A similar

high and constant thermal regime was assumed to apply equally to Crocodylus species

(Hutton and Webb, 1992), and has been applied in captive situations for C. porosus

(Davis, 2001; Mayer, 1998), Crocodylus niloticus (Hutton and Van Jaarsveldt, 1987)

and Crocodylus siamensis (Lang, 1987). However, there have long been concerns that

some fundamental differences may occur between A. mississippiensis and other

species, and that a more variable thermal environment may be more appropriate for

some crocodilians (Lang, 1987). Captive Alligator sinensis, despite being genetically

close to A. mississippiensis, have poor survival and growth rates at constant

temperature and need to experience winter cooling to maintain good health (Herbert et

al., 2002).

In this study we describe the thermal preferences that hatchling C. porosus exhibit

under controlled laboratory conditions in a thermal gradient and test the hypotheses

that the temperatures selected by hatchlings are not subject to a daily rhythm, and are

not affected by state of feeding or social aggregation (being in a group).

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2. Materials and Methods

2.1 Animals and husbandry

In July-August of 2011, 48 captive-born C. porosus hatchlings, 3-4 months of age,

were obtained from Wildlife Management International (WMI), Darwin, Australia.

Hatchlings originated from 19 clutches collected from the wild (2-30 days old when

collected), and from captive bred stock, and had been artificially incubated at 32 ºC

and 95-100 % humidity. All were raised in the same conditions, with constant water

temperature (32 ºC), and air temperature fluctuating a few degrees higher during the

day than at night. The mean size of hatchlings, when released into the laboratory

gradients at Charles Darwin University, was 214.0 ± 10.0 mm SVL (SD; 190 to 230

mm), 456.6 ± 20.6 mm TL (SD; 410 to 490 mm) and 263.3 ± 35.3 g body mass (SD;

201 to 321 g). Individuals were housed in isolation (N=16) or in groups of four

individuals (N=8 groups). Given that all animals had been subjected to the same

thermal environment from hatching, no period of acclimation at a constant

temperature was considered necessary to counter effects of the previous thermal

history on preferred temperatures (Heatwole et al., 1975).

Experimental enclosures which served as thermal gradients were comprised of glass

tanks (115 cm x 65 cm x 50 cm high) propped up on one end (10 cm high) to create

an area of land (32.5 cm x 57.5 cm) that gradually sloped down to an area of water

(32.5 cm x 57.5 cm x 5 cm deep). They were in a temperature controlled room (22 ± 1

ºC) with a 12:12 h light:dark cycle (light 0700 to 1900h). Two ceramic heating

222

elements (150 W and 250 W, Oz Black URS®) were arranged at different heights in

each enclosure to establish an approximately linear temperature gradient on the land

(22-45 ºC). Air and water temperatures were measured throughout the experiment

using temperature data loggers (Thermocron iButtons®) and remained stable at 22 ±

0.5 ºC with no daily fluctuations. This range of temperatures is that what hatchling C.

porosus in northern Australia are exposed to in the wild (Webb et al., 1978), and is

similar to the range used in the thermal gradient studies of Lang (1987). To ensure

hatchlings were not simply using the heating ceramics as cover, several other

ceramics, not connected to power, were placed throughout the tank. The use of

ceramic heat sources, rather than heat lamps, allowed shuttling between land and

water (Grigg and Seebacher, 2000; Seebacher and Grigg, 1997) without

compromising the diurnal light cycle.

The sides of each tank were covered in thin black plastic to restrict visual contact

between adjacent tanks. Preliminary observations, using infrared CCTV cameras

(Signet® IR wide angle) prior to the experiment revealed that individuals settled and

began shuttling between warm and cooler areas within 24-35 hours. Observations of

behavior were collected during the experiment using cameras mounted in the pens and

connected to a digital video recorder (Signet® 4 CH-DVR, model QV-3020).

2. 2 Procedure and protocol

All 48 hatchlings were force-fed temperature data loggers (Thermocron iButtons®).

Each iButton® (12 x 4 mm) was coated with a thin layer of inert liquid plastic

223

(Performix® Plasti dip). The package weighed 3 g and constituted < 1.5% of

hatchling body mass. Each iButton® was calibrated against a mercury-in-glass-

thermometer traceable to a standard, before and after each experiment. Loggers were

programmed to record body temperature at hourly intervals. Crocodilians typically

retain hard objects in their stomach (e.g. gastroliths) and all iButtons® remained in

place until removed at the end of the experiment by stomach flushing (Taylor et al.,

1978). Force-feeding and removal of the iButton® took less than 30 s and appeared to

cause minimal distress to the animals.

To ensure individuals were in a post-absorptive state when the experiments started,

they were fasted for 24 h before release into the pen and allowed 48 additional hours

to settle. For several species of crocodilians, digestion is essentially complete within

48 h of feeding at or near optimal Tb (Coulson and Hernandez, 1979; Garnett and

Murray 1986). Body temperature data over 24 hours (day 3: 0900 h - day 4: 0900 h)

was used to establish initial baseline thermal preferences for each individual, while

fasted, in both isolated (N=16) and group treatments (N=32).

On day 4 (1000 h), randomly chosen hatchlings from the isolated treatment (N=8)

were force-fed a meal of minced red meat, equivalent to 7% of each individual’s body

mass (mean: 18 g), which was considered a satiation meal (Davenport et al., 1990).

The interference involved in force-feeding was undesirable but considered essential to

ensure ‘fed’ animals had all eaten a similar amount of food, and that the amount of

food eaten was considerably greater than the mass of the loggers (3 g). To account for

the potential affect of handling, fasted individuals in the isolated treatments (N=8)

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were subjected to the same force-feeding procedure, but the food was withheld (sham

feeding). Body temperatures from 1100 h on day 4 through to 1100 h on day 5, were

used to test differences in Tb between fasted and fed individuals in the isolated

treatment. All experiments were then terminated. Three of the hatchlings in isolation

(fasted) and three groups of hatchlings were filmed during the 24 h period from 0900

h on day 3 to 0900 h on day 4 to quantify activity cycles. The number of times each

individual moved between land and water was recorded. For the group treatments, the

total number of movements observed in an hour was divided by the number of

animals (N=4). Animals in the social groups were neither fed nor subjected to sham

feeding.

2.3 Statistical analyses

The majority of results are presented as mean Tb with one standard deviation (SD) to

indicate thermoregulatory precision (Khan et al., 2010), and N is provided to allow

calculation of standard errors. Where appropriate, thermoregulatory set point range

(Tset: central 50% of Tbs recorded) and the voluntary thermal minimum (VTmin) and

maximum (VTmax) temperature (Hertz et al., 1993; Huey, 1982) are reported.

Distributions of Tb for individuals and groups showed a high degree of normality

(Shapiro-Wilk’s test) and homoscedasticity (Cochran’s test). A paired t-test (Sokal

and Rohlf, 1995) was used to compare mean Tb and variation (SD) on the same

individuals in isolation before and after feeding (and sham feeding). A repeated

measures ANOVA (mean Tb) and an ANOVA (variation: SD) was used in

comparisons between individuals in isolation that were force fed and sham fed, and

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between individuals in the isolated and group treatments. An ANOVA was used to

compare mean Tb and variation between active (1100-1700 h) and less active (1800-

1000 h) periods for the same individuals. A significance level of α = 0.05 was used

for all statistical tests. Statistical analyses were performed using JMP 8.0 statistical

software (SAS Institute Inc., 2010).

3. Results

3.1 Behavior

Hatchlings in the gradients displayed classic thermoregulatory behavior, shuttling

between the warm (land) and cooler (land and water) sections of the gradient. When

on land, they were rather inactive, tending to lie flat on the ground in one place, and

then after a time, move to another site (warmer or cooler) and settle. This inactivity

was particularly obvious between 1100 to 1700 h (quiescent period, QP), and

independent of whether individuals were housed in isolation or in groups. Activity

levels were higher at other times (see below; non-quiescent period, NQP), and

markedly so at dusk and early evening. When in water, which was cool (22 ºC),

hatchlings were constantly active and moving before returning to the land.

When on land, individuals that approached the radiant ceramic heaters oriented their

head and anterior trunk towards the heat source. After a period they re-adjusted their

position so the tail and lower trunk were closest to the heater. If positioned in a less

extreme part of the heated area (32-34 °C), they often moved to a cooler section of the

226

land surface (26-28 °C) or adopted a position with part of the body on land and part in

the water. If lying in the warmest section (42-45 °C) of the gradient, or orienting close

to the heat source for a prolonged period, they typically moved directly into the water.

In the group treatments, individuals often lay together, in contact with each other on

parts of the land surface (warm or cool), particularly during the QP. Despite some

aggressive interactions, mainly around dusk and dawn (head strikes and assertive

displays), no individuals appeared to be actively or aggressively excluded from any

section of the gradient by other individuals, as judged by viewing the videos.

3.2 Mean Body Temperatures

The same individual C. porosus in isolation had similar mean Tb’s with similar

variation (SD) the day before force feeding (FF-1: day 3) or sham feeding (SF-1: day3),

and after FF and SF (day 4), and there were no significant differences between FF and

SF treatments (day 4) (N=8 each; Table 1 and 2). There was no significant difference

in mean Tb or variation between the treatment in which individuals were housed in

isolation (N=16) and the treatment in which individuals were housed in groups

(N=32) (Table 1 and 2).

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Table 1. Mean of mean body temperatures (Tb) (SD and N), set point range

(Tset), and voluntary maximum (VTmax) and minimum (VTmin) for individual C.

porosus in isolation in the force fed (FF-1, FF) and sham fed (SF-1, SF)

treatments, and individuals housed in isolation (fasted; N=16) and individuals

housed in groups (fasted: N=32) in a thermal gradient (22-45 ºC).

Treatment Mean Tb SD N Tset VTmax VTmin

FF-1 30.9 2.2 8 29.2-32.6 37.1 25.1

FF 30.8 2.3 8 29.5-32.4 37.4 24.5

SF-1 30.5 2.3 8 28.7-32.2 36.5 24.7

SF 30.5 2.5 8 28.9-32.2 38.3 23.7

I 30.7 2.3 16 29.1-32.2 37.1 24.7

G 31.1 2.3 32 29.6-32.6 37.6 23.2

FF = force fed, SF = sham fed, FF-1 and SF-1 indicates the FF and SF animals

in isolation 1 day before feeding. I = individuals housed in isolation (fasted),

G = individuals housed in groups (fasted).

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Table 2. Comparisons of mean (paired t-test or repeated measures ANOVA) and

variation (paired t-test or ANOVA) in Tb between individual C. porosus in isolation

in the force fed (FF-1, FF; N=8) and sham fed (SF-1, SF; N=8) treatments, and

individuals housed in isolation (fasted; N=16) and housed in groups (fasted; N=32),

in a thermal gradient (22-45 ºC).

Treatments Mean Variation

FF-1 and FF t = 0.67, df = 191, P = 0.50 t = -1.04, df = 7, P = 0.33

SF-1 and SF t = -0.59, df = 191, P = 0.56 t = 0.23, df = 7, P = 0.82

FF and SF F1,14 = 0.73, P = 0.41 F1,14 = 0.49, P = 0.50

I and G F1,46 = 1.84, P = 0.18 F1,46 = 0.01, P = 0.94

FF = force fed, SF = sham fed, FF-1 and SF-1 indicates the FF and SF animals

in isolation 1 day before feeding. I = individuals in isolation (fasted), G =

individuals in groups (fasted).

As there was no statistical differences between treatments, Tbs from individuals in a

post absorptive state (day 3) from both the isolated (N=16) and group (N=32)

treatments were combined to give an overall mean Tb of 30.9 ± 2.3 ºC (SD; N=1152).

Fifty percent of Tbs (Tset) were between 29.4 ºC and 32.6 ºC, and the voluntary

maximum (VTmax) and minimum (VTmin) temperatures were 37.6 ºC and 23.2 ºC

respectively.

3.3 Cyclic Body Temperatures

Although mean Tb (Tables 1 and 2) provides a general index of preferred temperature

229

and the effects of feeding and social aggregation on it, at a finer level of resolution the

situation is more complicated. In the thermal environment provided, Tbs of individual

C. porosus fluctuated on a pronounced diurnal cycle (Fig. 1a,b) with significantly

higher Tbs during the QP (1100-1700 h) compared with the NQP (I: F1,382 = 35.42, P

< 0.5; G: F1,766 = 45.22, P < 0.5), with the lowest hourly Tbs during the early morning

(0600-0700 h). Mean Tb was similar during the QP and NQP regardless of treatment

(Table 3).

Fig. 1. Mean Tb (±SE) as a function of time of day, for individual C. porosus housed

in (a) isolation (N=16) and in (b) groups (N=32) in a post-absorptive state in a

thermal gradient. The thin horizontal line is the mean value across all hours and the

230

heavy bar indicates the quiescent period (QP).

Table 3. Comparisons of mean Tb (paired t-test or repeated measures ANOVA)

during the QP and NQP between individual C. porosus in isolation in the force fed

(FF-1, FF; N=8) and sham fed (SF-1, SF; N=8) treatments, and individuals housed in

isolation (fasted; N=16) and individuals housed in groups (fasted; N=32) in a thermal

gradient (22-45 ºC).

Mean Tb

Treatment groups Quiescent period Non quiescent period

FF-1 and FF t = 0.48, df = 55, P = 0.64 t = -1.48, df = 135, P = 0.14

SF-1 and SF t = -0.28, df = 55, P = 0.79 t = -0.45, df = 135, P = 0.65

FF and SF F1,46 = 0.16, P = 0.70 F1,46 = 0.81, P = 0.38

I and G F1,46 = 0.18, P = 0.67 F1,46 = 2.8, P = 0.10

As there was no statistical differences between treatments, Tbs from individuals in a

post absorptive state (day 3) from both the isolated (N=16) and group (N=32)

treatments were combined to give a mean Tb of 31.9 ± 2.09ºC during the QP and a

mean Tb of 30.6 ± 2.31ºC during the NQP. However, upon further inspection there

was a significant difference in Tbs (F1,46 = 9.52, P < 0.05) between individuals in the

isolated and group treatments just prior to the QP (0600-1100 h). During this period,

individuals in groups maintained Tbs slightly higher (1.2°C) than individuals in

isolation (Fig 1a,b).

Variation in Tb (SD) was not significantly different between the QP and NQP for

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individuals housed in isolation (F1,22 = 0.04; P = 0.85) or individuals housed in

groups (F1,22 = 1.91; P = 0.19), although Tbs were more variable at dusk and early

evening (Fig. 2a,b).

Fig. 2. Variation in Tb (SD) as a function of time of day, for individual C. porosus

housed in (a) isolation (N=16) and in (b) groups (N=32) in a post-absorptive state in a

thermal gradient. The thin horizontal line is the mean value across all hours and the

heavy bar indicates the quiescent period (QP).

During the QP individual C. porosus in the isolated (N=16) and group (N=32)

treatments were relatively inactive (I: 2.3 ± 1.46 movements/h; G: 2.0 ± 1.53

232

movements/h) and on land thermoregulating (Fig. 3a,b) whereas during the NQP

individuals were more active (I: 6.2 ± 2.39 movements/h; G: 5.0 ± 2.40 movements/h;

Fig. 3a,b). Activity increased rapidly for individual C. porosus housed in the isolated

(N=16) and group (N=32) treatments immediately after the QP, at dusk and early

evening (1800-2000 h; Fig. 3a,b), when mean Tb declined and variation (SD) was

highest (Fig. 1a,b; 2a,b). The variability in Tb and activity (movements/h) throughout

the day could not be explained by any changes in ambient temperature, which

remained constant across the 24 h period (22.0 ± 0.5 ºC).

Fig. 3. Activity (mean movements per hour ±SE) as a function of time of day,

observed for three individual C. porosus housed in (a) isolation and for three (b)

233

groups of four individuals in a post-absorptive state in a thermal gradient. For the

groups of individuals, the total number of movements in an hour was divided by the

number of animals (N=4). The thin horizontal line is the mean value across all hours

and the heavy bar indicates the quiescent period (QP).

4. Discussion

The Tbs of hatchling C. porosus in this study were broadly similar to those reported

for other species of crocodilian (30-34 ºC) of similar size, measured in thermal

gradients, including C. novaeguineae (Lang, 1981), C. crocodilus (Diefenbach, 1975),

C. siamensis (Lang, 1987), and A. mississippiensis (Lang, 1976). Alligator

mississippiensis is a temperate species of crocodilian that sometimes operates at lower

ambient temperatures than most other crocodilians (Brandt and Mazzotti, 1990). The

mean preferred body temperatures sought by crocodilians appear similar across

species, despite the ability to sustain those temperatures no doubt being affected by

prevailing thermal conditions as affected by season, time of day and geographic

location (Andrews, 1998; Bury et al., 2000; Tracy and Christian, 1986). Hence,

performance in a thermal gradient is likely to provide different insights into preferred

Tb than those obtained by measuring Tb of crocodilians in the wild.

Hatchling C. porosus in this study maintained similar Tbs and thermal precision

regardless of whether they were fasted or fed, as reported for C. crocodilus

(Diefenbach, 1975) and C. novaeguineae (Lang, 1981). We could not reject the

possibility that the data loggers (3 g) could have triggered a feeding response in all

234

animals, even though the fed animals received 18 g of food. Alligator mississippiensis

and C. acutus selected higher and less variable Tbs after feeding, although the

response was less pronounced in C. acutus (Lang, 1979). It has been suggested that

the postprandial thermophilic response may be more important for species, such as A.

mississippiensis, that inhabit temperate climates with more variable seasonal

fluctuations in ambient conditions (Lang, 1979; 1987). For crocodilian such as C.

porosus that inhabit tropical climates with relatively constant, year-round warm

temperatures, the need to increase Tb in response to feeding may be unnecessary,

given that ambient conditions can generally be expected to be suitable for digestion

(Lang, 1979; 1987).

In our study, just prior to the QP (0600-1100 h), animals in groups maintained Tbs

slightly higher than individuals in isolation. This difference was minor, and may

reflect grouped animals, with their lateral surfaces often in contact with each other,

heating and cooling more slowly due to changes in the exposed surface area to mass

ratio and its affects on relative insulation. Little biological significance is attached to

this finding.

Individuals in a group basked together, and although aggression was observed, it was

never intense enough to exclude individuals from any section of the gradient. This

suggests that thermoregulation in hatchling C. porosus may not be affected by

agonistic behavior to the same degree as reported for juveniles and adults of several

species, where less dominant individuals were actively excluded (eg. chased) from

optimal thermal habitat by larger animals, and as a consequence had lower and more

235

variable Tbs (Grigg et al., 1998; Johnson et al., 1976; Lang, 1987; Seebacher and

Grigg, 1997). While aggression among hatchling C. porosus may lead to temporary

displacement, hatchlings appear to be largely tolerant of each other when

thermoregulation appears to be a priority for all individuals (basking during the QP).

The general daily cycle of body temperatures reported here, although less pronounced,

is similar to that reported for sub-adults and adults of several crocodilian species

studied in semi-natural enclosures, or in nature (Downs et al., 2008; Grigg et al.,

1998; Seebacher, 1999). In those studies, diurnal variation in ambient temperatures

was an obvious cause of the observed changes in Tb. In our study, Tbs of hatchling C.

porosus were 1-2 ºC higher during the day than at night with over 3 ºC separating the

peak high temperatures (1100-1700 h) from the peak low temperatures (0600-0700 h).

Lower body temperatures at night were correlated with increased activity and time

spent in the water, but activity alone could not explain the peak trough in Tb in the

early morning (0600-0700 h), when for some reason, hatchling C. porosus prefer

lower Tbs.

Because hatchling C. porosus have a behavioral tendency to be in the water at night,

the constant low water temperature (22 ºC) provided in our gradient may have

encouraged lower preferred Tbs than would be adopted if a higher water temperature

had been available. Other gradient studies with hatchling and juvenile crocodilian

species have not reported any clear daily cycle in thermal preference to date (Lang,

1979; 1981). However, these studies involved a temperature gradient in both the water

and on land (Lang, 1979) which could dampen any variation that did exist. Juvenile A.

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mississippiensis within a gradient preferred to remain in the heated water during the

day, rather than basking on land, despite land basking being a normal and common

behavior in the wild (Lang, 1979). Wild juvenile C. porosus have appreciably higher

food conversion rates than their captive counterparts, which could also be partly

explained by reducing Tb (and maintenance costs) when possible (Webb et al., 1991).

Voluntary night time hypothermia has been observed in some lizards, perhaps for the

same reason (Christian, 1986; Huey, 1982; Regal, 1967).

The increase in activity around dusk and early evening (1800-2000 h), which

introduced more variability in Tb, has also been reported in several crocodilian species

(Lang, 1987). It appears to reflect obligations to forage, but if the risk of predation on

hatchlings by diurnal predators is high, it may also reflect predator avoidance.

The overall mean Tb (31.0 ± 0.07 °C) of three month old hatchling C. porosus in this

study was slightly lower than that reported for both hatchlings less than 10 days old

(33.2 ± 0.3 °C; N=6) within an indoor enclosure (Lang, 1981), and for free-ranging

adults and sub-adults in a natural enclosure during the summer (28.4-33.6 °C, N=11;

Grigg et al., 1998; 32-33.1 °C, N=14, Johnson et al., 1976). However, the differences

were less if only Tb during the QP (31.9 ± 2.09 ºC) is considered as the best index of

preferred Tb. Thus, while thermoregulatory behavior of C. porosus no doubt changes

with increasing size (Spotila et al., 1972), altering the time taken to heat and cool,

preferred temperature does not appear to vary greatly with increasing size, as found

for C. niloticus, A. mississippiensis, and C. novaeguineae (Lang, 1987). Similar

preferred temperatures across sizes is also found in other large reptiles, such as

237

Komodo dragons (Varanus komodoensis), in which body size changes dramatically

between hatching and adulthood (Harlow et al., 2010).

In captivity, hatchling C. porosus exhibited higher growth and survival rates when

raised at a temperature experienced during incubation (Webb and Cooper-Preston,

1989; Webb et al., 1991), relative to either lower or higher constant temperatures

(Davis, 2001; Mayer, 1998; Webb et al., 1991). However, the current common

practice of raising hatchling C. porosus at constant warm temperatures (32-34 ºC air

and, or water) may not be optimising body temperature regulation and could be

constraining growth and survival rates (Licht, 1973; Wilhoft, 1958). Experimentation

with more variable thermal regimes, in the form of gradients or fixed temperature

cycling within the Tset range would seem warranted.

Acknowledgements

We thank Charlie Manolis and Jemeema Brien for their help in different phases of the


supply of animals, and for logistical support. WMI funding through the Rural

Industries Research and Development Corporation is gratefully acknowledged.

Funding for equipment was provided through a Holsworth Wildlife Research

Endowment (ANZ Trustees Foundation), Charles Darwin University, and a Northern

Territory Research and Innovation student grant. Experimental protocols were

approved by the Charles Darwin University Animal Ethics Committee, Darwin

(Animal ethics permit number A11003).

238

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Chapter 5.1. Out of sight or in too deep: effect of visual barriers and

water depth on agonistic behaviour and growth in hatchling


Published as: ‘Brien, M.L., Gienger, C.M., Webb, G.J., McGuinness, K.A., Christian,

K.A., 2014.Out of sight or in too deep: effect of visual barriers and water depth on

agonistic behaviour and growth in hatchling saltwater crocodiles (Crocodylus

porosus)’. Animal Behaviour Science: in press. Formatted according to author


Abstract

This study tests the role of visual barriers and water depth on levels of agonistic

behaviour and growth in hatchling Crocodylus porosus within the first 3 weeks of life.

Ninety-six individuals from four separate clutches hatched over 2 days were divided

across three treatments containing two groups with 16 individuals each: shallow water

with no visual barrier (SW), shallow water with visual barriers (VB), and deep water

with no visual barrier (DW). Body mass (BM-g) was measured at introduction and

after 21 days, and was used as an index of growth. Behaviour was described and

quantified in the night (17:00-8:00 h), when there is an innate peak in behavioural

interactions, for three consecutive nights on two occasions (days 9-11 and 18-20 post-

hatch). Visual barriers in open shallow water (VB: mean 0.7 interactions/night) nearly

eliminated agonistic behaviour relative to SW (mean 10.8 interactions/night; P <

0.05). DW did not reduce the frequency of agonistic interactions relative to SW, but

247

did affect the outcome of interactions (P < 0.05), with both individuals swimming off

slowly. The distribution of hatchling growth after 21 days was highly bimodal

regardless of treatment, with a group of slow growing (-3.6 to <6 g change in BM)

and fast growing hatchlings (6-15 g increase in BM). Although this made statistical

comparisons difficult, there was no clear effect of any treatment (P < 0.05) on mean

growth rates. The results of this study suggest that there may be utility in providing

hatchling and juvenile C. porosus in captivity with a more complex raising

environment in order to reduce negative social interactions, but it is not clear whether

this improves growth and survival.

Keywords: Crocodylus porosus, hatchlings, agonistic behaviour, growth, visual

barriers, water depth.

1. Introduction

Many species in captivity face a range of environmental and social challenges

which can cause stress and lead to a reduction in survivorship (Kristiansen et al.,

2004; Morgan and Tromborg, 2007). In farming situations, individuals often have to

contend with restricted space, higher than natural densities, and insufficient cover or

places to hide (Morgan and Tromborg, 2007). How well a species is able to adapt to

captivity is dependent upon the level of intraspecific aggression and tolerance to

conspecifics, and the complexity of the raising environment itself (Price, 1999;

Kristiansen et al., 2004).

The structure and complexity of the habitat has a strong influence on the social

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behaviour of many animals, especially in captivity (Petren and Case, 1998; Price,

1999). The use of artificial cover objects, dividers, and barriers have been successful

in reducing the frequency and intensity of agonistic interactions in several groups of

captive animals, including fish (Kadry and Bareto, 2010), pigs (McGlone and Curtis,

1985), red deer (Whittington and Chamove, 1995), chickens (Estevez et al., 1998;

Cornetto et al., 2002), goats (Aschwanden et al., 2009), and macaques (Estep and

Baker, 1991). Cover objects and barriers enable less dominant individuals to escape or

avoid such interactions (Price, 1999), which can in turn result in improved rates of

growth and survival.

In the wild, hatchling crocodilians typically occupy habitat at the water’s edge that

provides a high degree of protective cover in the form of vegetation, logs, and

branches (Mazzotti et al., 2007). Hatchlings use the complexity of their environment

to hide from predators, locate prey, regulate body temperature, and to possibly avoid

negative social interactions, as has been suggested for other species of animal (Estep

and Baker, 1991; Cornetto et al., 2002). However, in captivity, hatchling crocodilians

have fewer options for protective cover, and are often forced together in smaller

spaces at higher densities than would be encountered in the wild (Hutton and Webb,

1992).

Agonistic behaviour among juvenile crocodilians, along with clutch of origin, has

been implicated in highly variable growth and survival rates in captivity

(Huchzermeyer, 2003), and this variation in growth is established within a few weeks

post-hatching (Hutton and Webb, 1992; Brien et al., 2013). Regular size grading is a

common strategy used by farmers to manage agonistic behaviour which alleviates the

stress placed on smaller crocodiles by removing larger more dominant ones (Riese,

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1991; Hutton and Webb, 1992). Another strategy is the provision of a hide or shelter

that covers a section (15-60%) of the raising enclosure which provides refuge and

may also reduce agonistic behaviour (Hutton and Webb, 1992; Huchzermeyer, 2003).

Although few published studies have examined the effectiveness of these strategies, it

is widely acknowledged that they are important in reducing stress and improving

growth and survivorship in juvenile crocodilians (Riese, 1991; Mayer, 1998;

Huchzermeyer, 2003).

The saltwater crocodile (Crocodylus porosus) is considered the most aggressive

and least tolerant of conspecifics, which affects their captive management (Lang,

1987; Brien et al., 2013a, 2013b, 2013c). In captivity, agonistic behaviour is present

shortly after hatching (within 2 days) and has been implicated in reduced rates of

growth and subsequent mortality of hatchling C. porosus through ‘runtism’ or ‘failure

to thrive syndrome (FTT)’ on crocodile farms in Australia (Onions, 1987; Isberg et

al., 2009; Brien et al., 2014). Agonistic interactions occur primarily between two

individuals during defined activity periods (dusk and dawn) in shallow, open water

areas of the pen (<8 cm), which also coincides with feeding (Brien et al., 2013a).

In this study, we test the hypotheses that the frequency and type of agonistic

interaction between hatchling C. porosus would not be affected by: (a) increasing the

environmental complexity in a way that restricts visual contact between individuals;

and (b) increasing water depth. We also used absolute growth (body mass - BM) of

hatchling C. porosus after the first few weeks post-hatching as a predictor of longer

term growth and survival (Brien et al., 2014).

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2. Animals, materials, and methods

2.1. Animals and housing conditions

In March of 2012, 96 captive-born hatchling saltwater crocodiles (C. porosus)

were obtained from Wildlife Management International (WMI; Darwin, Australia).

They originated from four clutches collected from the wild (embryo age at collection

for each clutch ranged between 2-30 days) that had been artificially incubated at 32º C

and 95-100% humidity. After hatching (16-17th March 2012), individuals remained in

the incubator (32º C) for 3 to 4 days which allows early detection of compromised

individuals (none found here).

On the 20th of March 2012, 24 hatchlings from each of the four clutches (N = 96)

were divided into six groups of 16, each group consisting of four individuals

randomly selected from each clutch. The groups were allocated randomly to six tanks,

two of which contained a ‘visual barrier’ with shallow water (VB), two had ‘deep

water’ without visual barriers (DW), and two had ‘shallow water’ without visual

barriers (SW), regarded as normal practice controls. For each animal, snout-vent

length (SVL - mm), and body mass (BM - g) were measured and a uniquely numbered

metal tag (Small animal tag 1005-3, National Band and Tag Co., Newport, Kentucky,

USA) was attached between the webbing on the rear right foot prior to release into the

tank.

Hatchlings remained in these treatments for 21 days, before recapture and

measurement on day 22 (11th April 2012), with change in body mass (g) for each

individual used as an index of growth. Food was withheld for 24 h prior to this second

set of BM measurements.

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Treatment groups were fed chopped red meat supplemented with di-calcium

phosphate (4%) and a multivitamin supplement (1%) at 16:00-17:00 h each day ad

libitum, with waste removed the following morning (8:00-9:00 h) when the water was

changed. Water temperature was 24-28° C when changed, but was heated and

maintained at 32-34° C by two aquarium heaters (300 W Hydor Theo®, Just

Hydroponics, Melbourne, Victoria, Australia) thereafter. Ambient air temperatures

varied from 26-34° C, which are within the preferred range for this species at this life

stage (Brien et al., 2012). There was a 9:15 h light:dark cycle, with treatment groups

exposed to low levels of natural light during the day (light: 08:00-17:00 h), and

complete darkness from late afternoon (17:00 h) through to early morning (08:00 h).

The plastic tanks used to house treatment groups were oval shaped (220 x 110 x 50

cm), with a land area (approx. 75 x 110 cm) that gradually sloped down to a water

area (approx. 145 x 110 cm) (1000 L Oval Water Tub, Reln Pty. Ltd., Ingleburn, New

South Wales, Australia; Fig. 1). In the SW and VB tanks, the water level ranged from

4-8 cm, while in the DW tanks it ranged from 8-18 cm which was achieved by

elevating the front of the tank. At this greater depth, hatchlings either could not stand

or had difficulty touching the bottom comfortably. A ‘hide area’ (Riese, 1991; Mayer,

1998) was provided in each enclosure, and was constructed with eight lengths (50 cm

long) of 10 cm PVC pipe strapped together and on legs, positioned so that it covered

equal portions of land and water (Fig. 1).

In the VB tanks, the visual barrier was a square frame (110 cm long x 100 cm

wide) constructed with lengths of 2.5 cm diameter PVC pipe on legs also made from

PVC pipe (15 cm high). A total of 14 interlocking sheets of 1 mm thick, black, high-

density polyethylene film (HDPE) (110 cm long x 10 cm tall) were suspended from

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underneath the frame so that they hung down at the waters’ surface. Seven sheets

were suspended length ways with slits in the top so that the other seven sheets could

slot in and run perpendicular forming a more or less evenly spaced pattern of 6 x 6

grids across the water surface (Fig. 1). The sheets were also extended to form a further

six half open spaces on each side of the frame (Fig. 1). From preliminary trials, these

visual barriers did not restrict movement with individuals able to swim underneath the

suspended sheets with ease. This setup also allowed a clear view from above for

filming.

Agonistic behaviour among hatchling C. porosus of this age, under captive

conditions, occurs almost exclusively in areas of open water (Brien et al., 2013).

Therefore, the barrier structure was placed in the water adjacent to the hide area of

PVC pipes in order to eliminate open water. The intention of the visual barrier

structure was to replicate conditions experienced in the wild, in which hatchling C.

porosus exist at the waters’ edge in amongst vegetation, logs, and branches that

provide both visual and physical separation from conspecifics.

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Fig. 1. Top view (a) of the shallow water and deep water (left side) and visual barrier

tanks (right side) and side view (b) of the shallow water and deep water (top) and

visual barrier tanks (bottom).

2.2. Behaviour

A wide angle infrared CCTV camera (96º angle QV-8104, Signet, Brisbane,

Queensland, Australia) was used in each tank to record behaviour on digital video

recorders (4CH DVR QV-8104, 25 frames/s, Quad Mode, Signet, Brisbane,

Queensland, Australia). A recording period lasted 15 h (17:00-8:00 h), and was

conducted on three consecutive nights for each treatment group (45 h each) under

complete darkness with infrared cameras enabling clear viewing. This time period is

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when the majority of agonistic interactions among hatchling C. porosus occur under

captive conditions (Brien et al., 2012; 2013). The recordings were taken 9 (8-10) and

18 (17-19) days after the crocodiles were placed in the treatment tanks and were

viewed and assessed the following day by the same single observer. For each

recording period (17:00-8:00 h) all agonistic interactions that occurred were recorded.

An agonistic interaction was any interaction in which aggression was signalled by

postures or actions by one or both individuals (Table 1; Fig. 2). For each interaction,

the behaviours exhibited, number of individuals involved and displaying aggression,

the intensity of interaction (low, medium, high), the location (water, hide, land), the

time, duration of interaction, and outcome were also recorded (Table 1; Fig. 2).

Table 1. Ethogram of behaviours used by hatchling C. porosus during agonistic

interactions (derived from Brien et al., 2013a).


Initiation

Rapid advance RA Series of short rapid advance movements

towards another individual while LIW.

Chase C Rapid movement toward another individual in a

LIW posture.

Posture

Low in water LIW Immobile with only the top of the head and back

above the water surface (Fig. 2a).

Inflated posture IP Immobile with upward extension of either the

front two or all four limbs, with neck and back

arched high and head and tail angled downward

(Fig. 2b).

Head and tail raised HTR Immobile with head and tail raised out of water

while back remains low. Head is usually parallel

to the water but can also be angled upwards

(Fig. 2c).

Head raised high

HRH

Immobile with upward extension of the front

two limbs pushing the head and chest high out

of the water on a ~45º angle while tail remains

low (Fig. 2d).

Mouth agape MA Immobile with mouth opened wide (in

combination with postures LIW, IP, HTR or

HRH; Fig. 2e).

Non-contact

movements

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Light jaw-clap LJC Rapid opening and closing of the jaws at the

water surface, often repeated several times (LIW

or IP posture; Fig. 2f).

Tail-wagging TW Undulation of the tail from side to side in either

a gentle sweeping motion or rapid twitching,

often repeated several times (all postures; Fig.

2g).

Contact movement

Head push HP Head is pushed in to an opponent, usually with

mouth closed (LIW or IP posture).


Side head-strike SHS Head is thrust sideways in to an opponent while

the mouth is either open or closed (all postures).

Tail-wag side head

strike

TWSHS Tail wagging occurs prior to a side head strike,

increasing the force of the impact (all postures;

Fig. 2h).

Tail-wag bite TWB Tail wagging occurs prior to a bite which

propels the individual in to an opponent with

force (LIW posture; Fig. 2i).

Aggressive

individual

One that advances toward another and, or that

makes physical contact with another.

Duration of

interaction

Measured from when an individual advances

rapidly toward another or makes contact,

whichever comes first, until agonistic

behaviours cease or an individual moves away.

Intensity of

interactions

Low Contact is made after individuals lying together

disturb each other when moving, or after one

swims into another underwater.

Medium One individual approaches another and initiates

an agonistic interaction.

High One individual approaches another and initiates

an agonistic interaction. High intensity

interactions are distinguished from medium

intensity interactions by the display of more

intense contact behaviours, either TWB or

TWSHS.

Outcome

Both stand ground Both individuals remain in the vicinity of each

other in LIW posture.

One swims off

slowly

One individual swims slowly away from the

other in a LIW posture.

Both swim off

slowly

Both individuals move slowly away from each

other in LIW posture.

One swims off

rapidly

One individual moves rapidly away from the

other individual in a LIW posture.

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Fig. 2. Postures, non-contact and contact movements, described in Table 1, displayed

by hatchling Crocodylus porosus during agonistic interactions (derived from Brien et

al., 2013).

2.3. Statistical analyses

Statistical analyses were performed using GenStat 12.2 statistical software (VSN

International Ltd, Hemel Hempstead, Hertfordshire, United Kingdom). For each

analysis the effect of treatment was examined as a three treatment x two replicate,

completely random design. For some count data diagnostic tests on residuals from an

ANOVA indicated that a square-root (of X+0.5) transformation on the counts was

appropriate before analysis. In such a case, treatment means were back transformed to

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original units. A split-plot ANOVA of growth data examined the effect of clutch.

Because the analysis of treatment was based on tank average data, the fact that

animals within tanks displayed bi-modal patterns in growth did not violate

assumptions of normality in the ANOVA. As there was a consistent behavioural

response by each treatment across all nights, the behavioural data from the two

recording periods (days 7-9 and 17-19) was combined for analysis. To account for

lack of independence over time, repeated measures ANOVA’s were used to examine

the effect of treatment on the mean number of agonistic interactions, number of

contacts per interaction, duration of an interaction, number of individuals displaying

aggression per interaction, and intensity (low: 1; medium: 2; high: 3). Pair-wise

comparisons were done using a protected Fisher's LSD procedure. A Chi-square test

was used to analyse the effect of treatment on the outcome of an interaction. Due to

insufficient data (total: 9 interactions), this analysis did not include the Barrier

treatment. Back transformed means are presented in each case, with transformed

means (±SE) also presented for significant results. A significance level of P < 0.05

was used for all statistical tests.

3. Results

3.1. Growth

There was no significant effect of clutch (F3,9 = 1.81; P = 0.22) or treatment x clutch

interaction (F6,9 = 0.21; P = 0.97) on hatchling growth of the animals. There was also

no significant effect of treatment on hatchling growth in BM (F2,3 = 1.17, P = 0.42).

Back-transformed mean growths for the VB, SW, and DW groups were 4.0, 4.0, and

258

4.2 g respectively. In fact growth of animals in all six tanks was similar (Fig. 3), and

appeared to demonstrate two distinct patterns of growth: animals that lost weight or

grew little (slow growing: -3.6 to <6 g change in BM), and those that grew rapidly (fast

growing: 6-15 g increase in BM; Fig. 3).

Fig. 3. Initial body mass and change in body mass after 21 days for hatchling

Crocodylus porosus in each of the six treatment groups (shallow water; visual barrier;

deep water). Individual dots represent individual animals.

3.2. Behaviour

Hatchlings in all three treatments were primarily active at dusk and dawn, which

coincided with feeding in which individuals would grab food from where it was

placed on land and retreat to the water to eat. In most cases, the frequency of agonistic

259

interactions was also higher during these times. Agonistic interactions involved only

two individuals at any one time. A square-root transformation was applied to the

number of agonistic interactions per night before analysis. The number was

significantly lower (F2,3 = 460.16, P < 0.05) among hatchlings in the VB treatment

(0.7) than among those in the SW (10.8) and DW (9.3) treatments. Transformed

means for VB, SW, and DW groups were 1.1 ± 0.10 SE, 3.4 ± 0.03 SE, and 3.1 ± 0.06

SE respectively.

The mean duration of an agonistic interaction did not differ significantly (F2,3 =

5.24, P = 0.11) across treatments in the analysis of square-root transformed data.

Back-transformed means were 12.6, 24.6, and 9.0 for treatments VB, SW and DW

respectively.

The mean number of individuals displaying aggression during an interaction (one

or both) did not differ significantly with treatment (F2,3 = 0.08, P = 0.92), with only

one individual displaying aggression in 56.6 % of interactions. Back-transformed

means for VB, SW and DW were 1.5, 1.4, and 1.4 respectively.

The mean number of contact movements made by an individual during an

interaction did not differ significantly across treatments (F2,3 = 8.33, P = 0.06), with

back-transformed means of 1.3, 1.9 and 0.9 for VB, SW and DW respectively.

The mean intensity of interactions did not differ significantly between treatments

(F2,3 = 2.43, P = 0.24), with 28.9% low, 27.7% medium, and 43.5% high intensity

interactions over all tanks. However, the outcome of an interaction differed

significantly between the SW and DW treatments (X2 = 196, df = 4, P < 0.05). The

majority of interactions in the SW treatments resulted in both individuals standing

their ground, while in the DW treatments most interactions resulted in both

260

individuals swimming off with some also resulting in one individual swimming off

rapidly (Fig. 4).

Fig. 4. Outcome of agonistic interactions between hatchling Crocodylus porosus

in the shallow water (N = 32) and deep water (N = 32) treatments over three

consecutive nights (17:00-8:00 h) at 9 days and 18 days post-hatching. Mean

percentages and SE.

4. Discussion

The results of this study demonstrate that the provision of a visual barrier in open

water areas reduced, and nearly eliminated (~90% reduction), agonistic interactions

among hatchling C. porosus in captivity during the first few weeks post-hatch.

Significant reductions in the frequency of agonistic interactions due to the provision

of visual barriers or cover have also been reported in captive populations of deer (60%

reduction; Whittington and Chamove, 1995), pigs (40% reduction; McGlone and

Curtis, 1985), bulls (87% reduction; Chamove and Grimmer, 1993), and macaque

monkeys (30-50% reduction; Estep and Baker, 1991).

261

In all of these studies, the barrier effectively increased the complexity of the

environment, making it difficult for individuals to view or encounter each other while

also providing escape options. In hatchling crocodilians, this situation is similar to

what they encounter in the wild, where they tend to occupy vegetation, branches, or

logs at or near the waters’ edge (Mazzotti et al., 2007). While this type of habitat is

important in providing shelter and prey (eg. shrimp, fish, insects) it would also

influence social interactions, as has been reported in lizards (Petren and Case, 1998).

While increased water depth did not reduce the frequency of agonistic interactions

between hatchling C. porosus, it did affect the outcome with one or both individuals

forced to swim off in the majority of interactions. Deeper water made it difficult for

hatchlings to engage in agonistic behaviour, as they were unable to touch the ground

and were forced to expend energy maintaining their position at the water’s surface. In

comparison, hatchling C. porosus in shallow water (<8 cm) were able to stand their

ground during encounters with less effort.

Despite the effect of visual barriers and deep water on the frequency and nature of

agonistic interactions, this was not associated with any difference in mean growth

between the three treatments. This suggests that visual forms of agonistic behaviour

may be unimportant in influencing rates of growth at this early life stage. However,

previous research has demonstrated that visual forms of agonistic behaviour in

hatchling C. porosus in captivity develop shortly after hatching and are important in

the formation of dominance hierarchies within the first year of life (Brien et al., 2013).

As a consequence, dominant individuals grow rapidly, while subdominants have

lower rates of growth and survival. Therefore, the effect of visual barriers and deeper

water levels on agonistic behaviour and rates of growth and survival may be either

262

delayed, or are more important among older hatchling and juvenile C. porosus in

which the frequency of agonistic interactions is higher (Brien et al., 2013).

Although the importance of visual displays during agonistic interactions has been

widely reported, many animals also employ chemical and vocal forms of

communication (Lang, 1987; Mason and Parker, 2010). Chemical signalling plays a

significant role in communication among many animals (Mason and Parker, 2010),

including several species of lizard (Duvall et al., 1979; Burghardt, 1977) and snakes

(Carpenter and Ferguson, 1977), which begins shortly after hatching. Although

chemical communication is poorly understood in crocodilians, they possess two sets

of semio-chemical glands (throat and cloaca) (Mason and Parker, 2010) that are

believed to be used by adult males in marking territories and deterring rivals (Herzog

and Burghardt, 1977). As chemical signals can be detected by the receiver in the

absence of the signaller (Gosling and Roberts, 2001), it is possible that chemical

signals may be used by hatchling C. porosus to communicate, among other things,

aggressive intent.

Vocalisations are considered to be important forms of communication among

crocodilians (Herzog and Burghardt, 1977; Lang, 1987), especially among hatchlings

which vocalise with each other and the mother to signal danger, and keep the crèche

together (Lang, 1987). As adult crocodilians use vocalisations during agonistic

interactions (Herzog and Burghardt, 1977; Lang, 1987), it is possible that hatchlings

may do the same. However, we did not record audio during this study.

Regardless of whether other forms of social communication are employed by

hatchling C. porosus, they may simply be a consequence of the factors driving

variation in growth trajectories, rather than their proximate cause. For instance,

263

genetics and conditions experienced during incubation (ie. the clutch affect) have long

been known to have a strong underlying affect on growth and survival in crocodilians

and may be the ultimate driver (Webb and Cooper-Preston, 1989). However, there

may also potentially be a wide range of other variables responsible that are associated

with the raising environment itself.

5. Conclusion

Although the provision of a more complex raising environment did not result in

improved rates of growth among hatchling C. porosus, it did reduce the frequency of

agonistic interactions which would reduce the incidence and severity of injuries

among hatchling and juvenile C. porosus in captive settings. However, the provision

of a more complex raising environment may be more important in improving growth

rates among C. porosus at higher densities or at a later age and size when agonistic

interactions are more frequent and intense.

Acknowledgements

We would like to thank Wildlife Management International for the supply of

animals, use of facilities and logistical support. WMI funding through the Rural

Industries Research and Development Corporation is gratefully acknowledged.

Funding for equipment (cameras, digital video recorders) was provided through a

Holsworth Wildlife Research Endowment (ANZ Trustees Foundation), a Northern

Territory Research and Innovation Board student grant, IUCN Crocodile Specialist

Group student grant, and Charles Darwin University. Funding was also provided

264

through ARC Linkage grant LP0882478 awarded to authors KAC, CMG, and

GJW. We would like to thank one of the reviewers, Bob Mayer, for his very generous

assistance with the statistical analyses. Experimental protocols were approved by the

Charles Darwin University Animal Ethics Committee (Animal ethics permit number

A11003).

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Chapter 5.2. Effect of density on growth, agonistic behaviour, and

activity in hatchling saltwater crocodiles (Crocodylus porosus)

Abstract

Hatchling C. porosus were raised (two replicates) in identical enclosures (1.5m2), in

different group sizes (5, 10, 20 and 30) giving four densities (3.3, 6.7, 13.3 and 20.0

hatchlings/m2; or 0.30, 0.15, 0.08 and 0.05m

2/hatchling respectively). Hatchlings

came from five different clutches, hatched on the same day, spread evenly between

treatments. Growth was assessed between 4 and 25 days of age, which is a reliable

indicator of post-hatching growth trajectories for this species. Clutch and initial body

mass (BM) had a strong influence on growth, with lower growth among the largest

hatchlings born. The highest mean growth in body mass occurred at 6.7/m2

(6.12±1.24g) and was lowest at the highest density (20.0/m2: -2.33±0.63g).

Behavioural observations taken every 10 minutes on day 19 (24 h period) confirmed

that hatchlings remained relatively inactive and hidden under cover for most of the

day, and were more active at night, with peaks at dusk and dawn. However, the level

of hourly activity (mean movements per individual per hour) was highest at densities

of 13.3/m2 (0.44±0.10) and 20.0/m

2 (0.43±0.09), compared with densities of 3.3/m

2

(0.15±0.07) and 6.7/m2

(0.12±0.07). Behavioural observations at 17:00-08:00h over

three days (days 17-19) revealed that the frequency of agonistic interactions (mean

per animal per night) was highest at the lower densities (3.3/m2: 1.70±0.16; 6.7/m

2:

1.20±0.06) and decreased with increased density (13.3/m2: 0.71±0.04; 20.0/m

2:

0.49±0.03). The results suggest that as density increases above 6.7/m2, growth in

hatchling C. porosus during the first three weeks begins to decline as activity

269

increases. However, at the lowest density (and group size: 5), one or two individuals

become dominant and grow large at the expense of the remaining hatchlings.

Management implications are discussed.

Introduction

Animals in captivity are subject to a range of environmental and social challenges

which can impact the well-being and fitness of individuals (Kristiansen et al. 2004;

Morgan and Tromborg 2007). How a species responds to changes in population

density under captive conditions is dependent upon the level of intraspecific

aggression and social tolerance (Browns and Orians 1970; Kristiansen et al. 2004).

Understanding the role of density in shaping behaviour, growth, and survival of a

species is essential for optimising production and improving animal welfare in captive

situations (Estevez et al. 2007; Rodenburg and Koene 2007).

Growth and survival of many animals (eg. fish, poultry, pigs, cattle) under captive

conditions is often reduced when raised at unnaturally high densities or group sizes

(Weng et al. 1998; Kristiansen et al. 2004; Estevez et al. 2007). However, how social

interactions and activity are affected by density or group size is inconsistent (Estevez

et al. 2007). Increasing group size can result in higher (Estevez et al. 1997; Fisher et

al. 1997), lower (Hughes et al. 1997; Estevez et al. 1997), or no change (Schmolke et

al. 2003) in the frequency of agonistic interactions in different species. A few studies

have examined the effect of group size or density on activity patterns, with lower

activity observed at higher densities in chickens (Estevez et al. 1997) and rabbits

270

(Morrise and Maurice 1997), but higher activity at higher densities reported in fish

(Holm et al. 1998; Kristiansen et al. 2004).

Stocking density is an important consideration when raising crocodilians in captive

situations, with low rates of growth and survival and high rates of injury and illness

associated with high densities (Webb et al. 1983; Elsey et al. 1990; Hutton and Webb

1992). However, most studies have tended to report no significant effects of density

on mean rates of growth or survival (Zilber et al. 1992; Webb et al. 1983; Garnett and

Murray 1986), but this is partly a result of extreme variation in individual growth

rates. These studies have also been confounded by different pen types, land to water

ratios, level and type of cover, group sizes, densities, species, sizes and ages, and

degree of temperature control (Riese 1991; Mayer 1998). Furthermore, clutch effects

have not always been adequately accounted for, despite their significant influence on

individual performance (Webb and Cooper-Preston 1989). In virtually none of these

studies has behaviour been considered.

The saltwater crocodile (Crocodylus porosus) is the largest species of crocodilian and

produces the most commercially valuable skin (Webb and Manolis 1989; Fuchs

2006). In the wild, most hatchling C. porosus exist in crèches of 30-80 individuals

with the parental female for the first two months of their lives (Webb et al. 1977),

although there are exceptions (Magnusson, 1979). After this they disperse, which is

generally considered a response to growing intolerance of each other (Webb and

Messel 1978). In captivity, hatchlings also have a strong tendency to group together

(Webb et al. 1994), despite agonistic behaviour, the frequency and intensity of which

271

is affected by clutch and increases with age during at least the first year of life (Brien

et al. 2013a). Agonistic behaviour has been implicated in reduced rates of growth and

increased mortality of hatchling C. porosus on crocodile farms in Australia (Riese

1991; Isberg et al. 2009).

The recommended density guideline for raising hatchling C. porosus during the first

few months of life is 10-15/m2 (Australian COP 2009), but this is based on general

experience rather than experimental results. Therefore, the objective of this research

was to quantify the effect of density on growth, behaviour, and activity in the

immediate post-hatching period, which is considered crucial in determining long term

patterns of growth and survival in C. porosus (Webb and Cooper-Preston 1989;

Hutton and Webb 1992; Brien et al. 2014).

Methods


In April of 2012, 129 captive-born hatchling C. porosus were obtained from Wildlife

Management International (WMI; Darwin, Australia). Hatchlings originated from five

clutches of eggs collected from the wild (embryo age: 2-30 days) that had been

artificially incubated at 32ºC and 95-100% humidity. After hatching, individuals

remained in the incubator (32ºC) for three days to assist in the assimilation of residual

yolk. On day four, hatchlings from each of the five clutches were randomly assigned

and transferred to experimental enclosures where they were assigned to one of four

272

densities (Table 1). In this experiment we did not separate density from group size,

with the same enclosure (size and shape) used to house different numbers of hatchling

C. porosus.

Table 1. Group size and density of hatchling C. porosus with and without

basking cage included.

Group

size

Number of

groups

Density

(hatchling per m2)

Density

(m2 per hatchling)

5 2 3.3 0.30

10 2 6.7 0.15

20 2 13.3 0.08

30 2 20 0.05

Experimental groups were housed in box-shaped concrete enclosures with a core pen

area of 1.5m2

(75 x 200 cm; walls 150 cm high), comprising a land area (0.6m2; 75 x

80 cm) that gradually sloped to a water area (0.9m2; 75 x 120 cm x < 19 cm deep).

Five lengths (80 cm long) of 10 cm PVC pipe strapped together and on legs were used

as a ‘hide area’ centrally positioned in the water (partly immersed) but overhanging

the land. To increase thermal options, an outdoor ‘basking cage’ (100 x 120 x 150 cm

high), accessible through a hole in the wall (10 x 20 cm), was attached to each

enclosure. The results confirmed that most time was spent in the core area of each

enclosure (1.5m2), which is used for all density analyses, and the extra area provided

by the basking cages was ignored.

Hatchling groups were fed chopped red meat supplemented with di-calcium

phosphate (4%) and a multivitamin supplement (1%) at 16:00-17:00 h ad libitum each

273

day, with waste removed the following morning (08:00-09:00 h) when the water was

changed. Water temperature was 24-28°C when changed (total 1h), but was heated

and maintained at 32-34°C by a gas hot water system. Ambient air temperatures

varied from 26-34°C throughout the day, and there was a natural light cycle. These

temperatures are within the preferred range for this species at this life stage (Brien et

al. 2012).

For each animal, snout-vent length (SVL - mm), and body mass (BM - g) were

measured and a uniquely numbered metal tag (Small animal tag 1005-3, National

Band and Tag Co.) was attached between the webbing on the rear right foot prior to

release into the enclosures. The increase in body mass (BM-g) for each individual was

used as an index of growth. Hatchlings remained in these treatment groups for a

period of 21 days, before they were captured and re-measured on day 22. Food was

withheld for 24 h prior to the second BM measurements on day 22. This initial post-

hatching period is critical in determining rates of growth and survival after 300 days

(Brien et al. 2014), and after several years in this species (Webb and Cooper-Preston

1989).

Behaviour


record behaviour on digital video recorders (Signet 4CH DVR QV-8104). A recording

period lasted 15 hours (17:00-08:00 h), and was conducted on two consecutive days

for each group (30 h per group). The recordings were taken 18 and 19 days after the

274

crocodiles were placed in the new experimental enclosures. When scoring the

observations, an agonistic interaction was defined as any interaction between

individuals in which intolerance was signalled by postures or actions by one or both

individuals (Brien et al. 2013a). The total number of agonistic interactions observed

and the total number of agonistic interactions divided by the number of animals was

calculated.

For each agonistic interaction, the duration and intensity was also recorded. The

intensity of an interaction was characterised as: low, medium or high (Brien et al.

2013a). Low intensity interactions appeared accidental, occurring when individuals

lying together appeared to disturb each other when moving, or if one swam into

another underwater. Medium and high intensity interactions appeared deliberate, with

one individual approaching another with the goal of initiating an agonistic interaction.

High intensity interactions were distinguished from medium intensity interactions by

the display of more intense contact behaviour (Brien et al. 2013a).

One group of hatchlings from each of the four densities was filmed during the 24h

period from 17:00 h on day 18 to 17:00 h on day 19 to quantify habitat use and rates

of activity. The number of animals that were observed moving (swimming or

walking) along with the position of each individual in the enclosure (land: exposed;

water: exposed; under hide: covering equal parts land and water; at entrance to

outdoor cage; inside outdoor cage) was recorded every 10 minutes. The total number

of movements observed in an hour and the total number of movements in an hour

divided by the number of animals was calculated.

275



Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro-


linear regression was used to examine the effect of initial BM on growth. An ANOVA

was used to examine the effect of density on growth with replicate (replicate

enclosure) and clutch as factors, and initial BM as a covariate. Significant effects were

investigated by Tukey’s pair-wise comparisons. A repeated measures ANOVA was

used to examine the effect of density on the mean number of agonistic interactions in

a night, and mean number of interactions per animal in a night, with replicate and the

number of nights as factors. A repeated measures ANOVA with replicate and number

of nights as factors was also used to examine the effect of density on the duration of

an agonistic interaction, and on the mean number of movements per hour and per

animal per hour. A Pearsons’ chi square test was used to compare the intensity of

agonistic interactions. A significance level of P < 0.05 was used for all statistical

tests. All means are reported ± one standard error (SE) with sample sizes (N).

Results

1. Habitat use

Hatchling C. porosus had a similar pattern of habitat use regardless of density and

276

used the basking cages rarely (Fig. 1). The majority of the time (44.0-56.9%)

hatchlings were concealed under the hide-boards which covered equal parts of both

land and water, and this was highest during the day (10:00-15:00 h; Fig. 1). As

density increased, the percentage of animals under the hide-board decreased slightly

(Fig. 1). Hatchlings spent more time on land (25.8-31.9%) than they did in water

(15.2-26.7%), except for those at a density of 20.0/m2 in which it was similar (Fig. 1).

The use of land and water was highest between dusk and dawn (16:00-09:00 h), with

few animals venturing out from underneath the hide-board during the day. Hatchlings

rarely used the outdoor cages (0-1.3%), but lay at the entrance (0.9-2.2%) between

dusk and dawn (16:00-09:00 h). However, the percentage of crocodiles that utilised

the cages or lay at the entrance was slightly higher at 13.3/m2 and 20.0/m

2 compared

with those at 3.3/m2 and 6.7/m

2 (Fig. 1).

277

Figure 1. Percentage of the time hatchling C. porosus in each density utilised each of

the five habitat types as a function of time of day (dawn: 06:00-09:00 h; day: 10:00-

15:00 h; dusk: 16:00-20:00 h; night: 21:00-05:00 h) as determined by locations of

hatchling C. porosus each 10 minutes. For each density only one replicate group was

observed for a 24 h period.

2. Growth

Initial BM had a significant effect on growth (linear regression: R2

=0.27; F=47.26;

P<0.05; N=129), which decreased with increasing BM, and this pattern was consistent

across all but the lowest density (Fig. 2).

278

Figure 2. The effect of density (3.3, 6.7, 13.3, 20.0/m2) and initial BM on growth in

BM (g) after 21 days.

Most hatchling C. porosus either lost weight (N=63; 49%) or put on little weight

(<5g; N=40; 31%) after 21 days (Fig. 2). Density had a significant effect on growth

(F2,4=19.55; P<0.05), which was highest among hatchlings at a density of 6.7/m2, and

lowest at a density of 20/m2 (Table 3).

279

Table 3. Mean growth in BM (±SE) of hatchling C. porosus according to density (3.3,

6.7, 13.3, 20.0/m2) after 21 days. Levels are based on the results of pair wise

comparisons: those with the same letter are not significantly different.

Density (per m2) N Mean SD Range Levels

3.3 10 1.34±2.22 7.02 -5.6-14.7 A

6.7 20 6.12±1.24 5.56 -2.2-17.8 A

13.3 39 2.60±0.86 5.37 -7.2-16.5 A

20 60 -2.33±0.63 4.87 -12.2-11.8 B

3. Agonistic interactions

Frequency

The overall mean number of agonistic interactions in a night increased significantly as

density increased (F2,4=22.37, P<0.05; Fig. 3a), while the mean number of

interactions per animal in a night decreased significantly with increasing density

(F2,4=183.23, P<0.05; Fig. 3). At the lowest density, the frequency of agonistic

interactions per night was lowest, while the frequency per animal in a night was

highest. The frequency in a night and per animal in a night was similar at densities of

13.3 and 20.0/m2.

280

Figure 3. Mean (±SE) number of agonistic interactions per animal in a night for

hatchling C. porosus raised under the same conditions at different densities with two

replicates for each density.

Intensity

The intensity of agonistic interactions decreased significantly as density increased

(X2=87.56, df=6, P<0.05), with fewer medium and high level interactions among

hatchlings at 13.3/m2 and 20.0/m

2 (Fig. 4). In the majority of cases, these higher

intensity interactions involved and were instigated by the largest hatchlings in the

group.

281

Figure 4. Percentage of agonistic interactions at different intensities (low, medium,

high) between hatchling C. porosus raised under the same conditions at different

densities with two replicates for each density.

Duration

The duration of agonistic interactions also decreased significantly with increased

density (F2,4=46.95, P<0.05), with the duration of interactions at 13.3/m2 (mean:

16.86±0.70 s, range: 3-31) and 20/m2 (mean: 11.88±0.57 s, range: 3-30) significantly

shorter compared with those at 3.3/m2 (mean: 28.98±1.4 s, range: 10-55) and 6.7/m

2

(mean: 35.35±1.3s; range: 12-62).

4. Activity

The mean number of movements/h increased with density (F2,4 =37.50, P<0.05; Fig.

5a), as did the mean number of movements/h per animal (F2,4=12.36, P<0.05; Fig.

5b). Activity (mean movements) was similar between hatchlings at 3.3/m2

and 6.7/m2,

282

and between hatchlings at 13.3/m2 and 20.0/m

2.

Figure 5. Mean (±SE) movements per animal per hour for hatchling C. porosus

raised under the same conditions at different densities with two replicates for each

density.

Activity was highest among hatchlings across all densities at around dusk (16:00-

20:00 h) and dawn (06:00-09:00 h), coinciding with increased use of land and water.

Hatchlings at the two highest densities (13.3, 20.0/m2) were observed during the night

moving around the perimeter and appeared to be looking for a way out, often pushing

into the corners of the pen. This ‘escape/circling’ behaviour was rarely observed

among hatchlings at the lower densities (3.3, 6.7/m2).

Discussion

The results of this study suggest that density has a strong influence on growth,

agonistic behaviour and activity in hatchling C. porosus in a captive situation during

283

the first few weeks post-hatching. Although there was a strong effect of clutch on

initial size and growth of hatchling C. porosus, mean growth was highest at 6.7/m2

and was lower at the highest density (20.0/m2). Based on predictions of hatchling C.

porosus survivorship to 300 days of age from growth in BM (g) 24 days post-hatching

made by Brien et al. (2014), this would result in survival probabilities of 70% at

6.7/m2, 48% at 13.3/m

2, 45% at 20/m

2, and 40% at 3.3/m

2.

Higher densities are often associated with lower rates of growth in hatchling and

juvenile crocodilians raised in captivity, despite several studies reporting no

significant effect of density (Garnett and Murray 1976). For C. porosus, one study

reported higher growth rates after five weeks (post-hatch) at a density of 10/m2

compared with 20/m2 (Riese 1991), and another involving 8-10.5 month old hatchling

C. porosus reported lower growth rates among smaller animals as density increased

from 1/m2 to 10/m

2 (Mayer 1998). Studies involving juvenile (>5 months old)

American alligators (Alligator mississippiensis; Elsey et al. 1990) and Broad-snouted

caiman (Caiman latirostris; Poletta et al. 2008) also found lower rates of growth at

higher densities. However, while these lower rates of growth at high densities have

been attributed to higher levels of stress; it is unclear as to the social mechanisms

associated with this response in crocodilians.

The saltwater crocodile is considered the most aggressive species of crocodilian, with

a very low tolerance of conspecifics (Lang 1987; Brien et al. 2013b,c). Agonistic

behaviour starts as early as two days post-hatch, with the frequency of agonistic

interactions increasing and the development of a well-defined dominance hierarchy

284

within the first year of life (Brien et al. 2013a). In this study, the highest frequency of

agonistic interactions per individual occurred among hatchling C. porosus raised at

the lowest density (3.3/m2). In these smaller groups, one individual grew large and

dominated resources such as food and water, while the other four remained small.

These larger animals were the most dominant and were almost always involved in

agonistic interactions, which were often deliberate and of a medium to high intensity.

As density increased, the frequency of agonistic interactions (per individual) between

hatchling C. porosus decreased. Interactions were less focussed and intense (low

intensity) and were resolved more rapidly (shorter duration) as most individuals that

were nearby would react to the altercation by fleeing which caused the combatants to

stop. Unlike at the lowest density, dominant individuals were unable to target others

aggressively, as there appeared to be too many animals in close proximity for

sustained, intense encounters to occur. This suggests that for hatchling C. porosus at

very low densities, agonistic behaviour may be responsible for reduced growth in less

aggressive or subdominant individuals, while at higher densities, the effect of

agonistic behaviour appears to be less important.

Although the results were not significant, another study involving hatchling C.

porosus reported slightly lower growth rates among hatchlings raised at the lowest

(2.5/m2) and highest (10/m

2) densities (Garnett and Murray 1986), with the highest

growth at 5/m2, similar to this study. Lower rates of growth at both the highest and

lowest densities have also been reported in lobsters (Chittleborough 1975; Ryther et

al. 1988), poultry (Estevez et al. 1997; 2002; 2003), pigs (Andersen et al. 2004), trout

285

and Arctic charr (Alanara and Brannas 1996), and mice (Davis 1958). This pattern of

behaviour is similar to that described in the ‘tolerance hypothesis’ model proposed by

Estevez et al. 1997, in which lower levels of agonistic behaviour are predicted at

higher densities as individuals are unable to dominate others as they would in low

density situations.

Although the gregarious nature of crocodilians during the initial post-hatching stage

makes them good candidates for high density farming situations, there appears to be

important species-specific differences. For example, rates of growth and survival of A.

mississippiensis are much higher than for C. porosus, even when they are raised under

identical conditions (Joanen and McNease 1976; Webb et al. 1994), and this has been

attributed to the higher levels of aggression and lower tolerance of conspecifics in C.

porosus compared with A. mississippiensis (Lang 1987; Hutton and Webb 1992;

Brien et al. 2013c). Studies with lobsters under captive conditions have also found

lower rates of growth and survival in species that are highly aggressive and have a

low tolerance of conspecifics (James et al. 2001). This suggests that highly aggressive

and intolerant species may not be suited to captivity. In order to improve growth and

survival in these species, it may be necessary to provide a more complex raising

environment (eg. cover, barriers, escape routes) and ensure optimal stocking densities

are maintained and adjusted as individuals increase in size in order to mitigate

negative social interactions.

The level of activity among hatchling C. porosus (per individual) increased at the

higher densities (≥13.3/m2) while growth rates declined. This increased activity

286

coincided with the display of a circling or escape behaviour that was not observed at

the lower densities (≤6.67/m2). Individuals would move around the perimeter of the

enclosure, primarily at dusk and dawn. This circling behaviour is usually only

observed among hatchling C. porosus during the first few days after individuals have

been introduced into a new enclosure (MB personal observation), and is considered

exploratory or stress-related. However, hatchlings at the higher densities in this study

continued to display this behaviour after 18 days, suggesting a sustained level of

stress. The lower growth at higher densities may reflect the energetic consequences of

increased activity. While increased activity at higher densities has also been observed

in captive raised fish (Kristiansen et al. 2004), activity levels are often reduced in

chickens at higher densities or group sizes (Estevez et al. 1997) and this is due to a

barrier effect created by the animals themselves (Newberry and Hall 1990).

Higher than optimal densities can cause increased levels of plasma corticosterone,

increased incidence of disease, and lower levels of growth among juvenile

crocodilians raised in captivity (Elsey et al. 1990; Huchzermeyer 2003). However,

while agonistic behaviour has often been implicated, especially in C. porosus, the

results of this study suggest that hatchling C. porosus may respond to higher than

optimal densities by increasing the level of activity and demonstrating escape

behaviour. This may also be the case for other species such as A. mississippiensis that

exhibit increased corticosterone levels at higher densities which is not associated with

an increase in agonistic behaviour (Elsey et al. 1990). In rats, higher densities are also

associated with increased levels of activity and escape behaviour, which has been

linked to elevated corticosterone (indicating stress), organ pathology and

287

immunodepression (Hurst et al. 1999).

Garnett and Murray (1986) reported that densities for hatchling C. porosus should be

based on available land area only, as they observed that this is where hatchlings spend

the majority of the time. However, observations were only made during the day and

experimental enclosures did not contain any cover for animals to hide under, which

resulted in individuals piling on top of each other in the corners of the pen. This issue

of piling has been reported in other earlier studies involving hatchling crocodilians

(Webb et al. 1983; Webb et al. 1994; Huchzermeyer 2003), before the importance of

providing cover was recognised (Huchzermeyer 2003).

Hatchling C. porosus in this study spent the majority of the time during the day

inactive and under cover (hide board), or basking on land near cover. However,

activity levels increased between dusk and dawn and this coincided with increased use

of exposed water and land areas in which individuals engaged in other important

behaviours such as feeding and social interaction. Therefore, we argue that

considerations of density involving hatchling C. porous should incorporate land and

water areas.

In this experiment we did not separate density from group size, with the same

enclosure (size and shape) used to house different numbers of hatchling C. porosus.

However, group size and density are often adjusted simultaneously in studies of farm

animals (Estevez et al. 1997; Morisse and Maurice 1997; Nicol et al. 1999; Dumont

and Boissy 2000), including those undertaken with crocodilians (Garnett and Murray

288

1986; Elsey et al. 1990). Although studies should aim to examine either density or

group size in isolation, there are inherent difficulties associated with this (eg.

adjusting pen shape and size) which have only recently been fully appreciated

(Christman and Leone 2007; Estevez et al. 2007). Because growth rates of hatchling

C. porosus within the first 3-4 weeks post hatch are known to influence long term

patterns of growth and survival (Webb and Cooper Preston 1989; Brien et al. 2014),

these results also have important implications for management.

Despite a large number of confounding variables, it appears that the optimal density

for housing hatchling C. porosus during the initial post hatching stage is around 10-

15/m2 which is in agreement with the current Australian code of practice (COP 2009).

However, just as there appears to be a maximum optimal density at which to raise

hatchling C. porosus of this age, there also appears to be a minimum, or at least a

minimum group size. Based on the results of our study, we would argue that a group

size of less than 10 animals encourages higher levels of aggression and dominance

which results in highly variable rates of growth and lower survivorship.

Acknowledgements

We thank Wildlife Management International for the supply of animals, use of

facilities and logistical support. WMI funding through the Rural Industries Research

and Development Corporation is gratefully acknowledged. Funding for equipment

(cameras, digital video recorders) was provided through a Holsworth Wildlife

Research Endowment (ANZ Trustees Foundation), Northern Territory Research and

289

Innovation Board student grant, IUCN-SSC Crocodile Specialist Group Student

Research Assistance Scheme grant, and Charles Darwin University. Experimental

protocols were approved by the Charles Darwin University Animal Ethics Committee


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Chapter 5.3. Factors affecting initial growth rates of captive

saltwater crocodiles (Crocodylus porosus) hatchlings in captivity:

food form and temperature cycle

Abstract

Growth trajectories of hatchling C. porosus established in the first few weeks of life

are key determinants of survival rates and thus of fitness. This study examines

whether this initial growth, at a constant temperature regime, is affected by food form

(minced red meat, long- and short-chopped red meat, and a variety of short copped

meat). It also tests within the same experimental enclosures whether the temperature

regime (constant: 32-34ºC, gradient: 28-34ºC, warm night: 32-34ºC, warm day: 32-

34ºC), when fed short-chopped red meat, significantly influences early growth.

Hatchling C. porosus were from several clutches (Feed: 3; Temperature: 5) and raised

(two replicates) in identical enclosures (1.5m2) in groups of 10 hatchlings (6.7

hatchlings/m2). Body mass (BM-g) was measured at introduction and after 21 days,

while behaviour (Food form: feeding; Temperature regime: habitat use) was observed

on days 18-20. Hatchling C. porosus fed a short chopped form of either red meat

(15.2±2.3 g) or a variety of meats (12.3±2.1 g) had higher growth in BM than those

fed the standard minced (8.4±2.4 g) form or long chopped form of red meat (3.5±1.9

g). Hatchlings appeared to be more efficient at consuming short chopped pieces of

meat than they were at consuming either mince, which they frequently lost in the

water, or long chopped pieces, which were dropped after some effort trying to

consume. Hatchlings provided with a temperature regime of constant warm

299

temperatures (constant: 6.4±2.0 g), a gradient of temperatures (gradient: 5.3±2.2 g), or

warmer night time temperatures (warm night: 7.8±2.2 g), had higher growth than

hatchlings provided with warm temperatures during the day only (warm day: -1.2±1.1

g). Hatchlings in the Warm day temperature treatment had access to temperatures

within the Tset (measured as the central 50% of Tbs voluntarily selected in a thermal

gradient) for only 16 hours of the day, compared with 24 hours a day for all other

treatments. The results of this study suggest that growth of hatchling C. porosus in

captivity can be improved by providing ‘bite’ sized pieces of meat instead of mince

and a thermal regime that enables 24 h access to temperatures within the Tset for this

species.

Introduction

Hatchling C. porosus in captivity are particularly sensitive to failure to thrive syndrome

(FTT) up until one year of age, which results in low rates of growth and survival

(Huchzermeyer 2003; Isberg et al. 2009; Brien et al. 2014). Mortality through FTT

during the first year of life is generally reported as 10-20% but can be as high as 50%

(Isberg et al. 2009). Despite a large number of unreported on-farm attention and trials,

in addition to formal research (eg. Garnett and Murray 1986; Riese 1991; Webb et al.

1992; Davis 2001; Mayer 1998; Isberg et al. 2009; Brien et al. 2012; 2013; 2014), the

cause of this syndrome remains largely unknown.

In captive environments, new born hatchling C. porosus are sensitive to the structural,

functional and management characteristics of their raising environment. There are

300

pronounced clutch effects in that sensitivity, which appear to be an interaction between

genetic predispositions and incubation history (Webb and Cooper-Preston 1989). The

success or otherwise of a raising strategy is largely reflected in the proportion of

hatchlings afflicted by FTT, which once started is difficult to reverse (Brien et al.

2014). This syndrome is apparent by the extent of individual growth in the first 24 days

post hatching, which is a good predictor of later growth and survival probabilities


In the wild, C. porosus live in communal groups (crèches) for at least the first two

months of life (Webb et al. 1991), and feed on a wide range of prey items, such as

crustaceans and arthropods, that are alive and moving (Taylor 1979; Webb et al.

1991). They crush, manipulate and swallow them whole, obtaining a reasonably large

amount of food for each unit of capture effort. The majority of feeding occurs around

the waters’ edge. In captivity, a number of studies have been dedicated to dietary

preference and feeding regimes of hatchling C. porosus (Garnett and Murray 1986;

Davis 2001). Hatchlings are typically fed a diet of red meat mince combined with

multivitamin and calcium supplements five to six days a week, in order to maximize

growth (Hutton and Webb 1992; Davis 2001).

The current temperature regime used for raising hatchling C. porosus on commercial

farms involves air and water temperatures being maintained at a constant 32-34ºC

(Webb and Manolis 1990; Mayer 1998). This was originally based on the American

alligator (Alligator mississippiensis) farm model and the optimal temperature used for

incubating C. porosus eggs (32ºC: Webb and Cooper-Preston 1989). However, the

301

merits of a constant thermal environment for hatchling C. porosus as used with A.

mississippiensis, relative to a cyclic or variable one, have not been examined and

remain unclear. It is important to note that the large majority of reptiles in captivity

are provided with some form of thermal gradient, and the importance of this variable

regime is widely recognised (Peaker 1969; Pough 1991).

In a recent study of hatchling C. porosus within a thermal gradient, preferred Tb’s

were not constant but cycled throughout the day (Brien et al. 2012). Warmer more

stable Tb’s were maintained during the day (11:00-17:00 h: 31.2ºC) when hatchlings

were less active and basking on land, with slightly cooler and more variable Tb’s

(18:00-10:00 h: 30.6ºC) during the night and early morning when hatchlings were

more active and in the water (Brien et al. 2012). While engaging in thermoregulatory

behaviour within a variable thermal regime may not be essential for maintaining

preferred temperatures per se in hatchling C. porosus, it could still play a role in

influencing rates of growth and survival.

Hatchling C. porosus that initiate feeding rapidly, and thus start to grow quickly, are the

least likely to suffer from FTT (Brien et al. 2014). So while the interactive causes of

FTT may still be unknown, manipulating food form or the temperature regime may be

ways of reducing this problem. The present study examines the effects of a) four

different thermal regimes (constant, gradient, diurnal heating, nocturnal heating) and b)

three different food forms (minced, short chop, long chop): on growth of new-born

hatchling C. porosus after 24 days, raised in otherwise identical enclosures, using the

same management and husbandry procedures and protocols.

302

Methods

Clutches, eggs and incubation

Eggs and hatchlings used in these experiments were provided by Wildlife

Management International (WMI; Darwin, Australia). Eggs came from both captive

(collected 1-2 days after laying) and wild nests (collected 1-25 days old after laying)

in the Northern Territory of Australia. Incubation was carried out (or completed)

artificially at constant 32ºC (±0.2ºC) and 98-100% humidity until hatching. Eighty

hatchling C. porosus from five clutches (4 wild; 1 captive bred) were used in the

thermal experiment, and a further eighty five from three clutches (1 wild; 2 captive

bred) were used in the feeding experiment. Clutches within each experiment hatched

within 1 day of each other (Thermal: 8-10th March 2012; Feeding: 19-21st March

2012), with those hatchlings that had deformities or obviously excessive yolk

excluded from experiments. Hatchling sex was not determined, but 32ºC is a male

producing temperature and the majority of eggs were incubated at this temperature

through the sensitive period for sex determination (Webb et al. 1987).

All hatchings were held in the incubator in crates for three days, which is thought to

assist the assimilation of residual yolk, before release into their raising enclosures on

day four. For each hatchling, a uniquely numbered metal webbing tag (Small animal

tag 1005-3, National Band and Tag Co.) was attached to the rear back right foot at the

time of hatching. Snout-vent length (SVL in mm to the anterior of the cloaca) and

303

body mass (BM in g) were also measured at four days of age when the animals were

introduced into the enclosures and again at 24 days of age. However, we used only

growth in BM as an index of performance, as previous studies involving hatchling C.

porosus have found this to be the most effective measure (Brien et al. 2014).

Experimental enclosures

Hatchlings in both experiments were raised in mixed clutch groups of 10-11

individuals under identical conditions from day four until day 24 post-hatching. The

enclosures were box shaped (170 x 100 x 50 cm high) and constructed of fibreglass

with a land area (70 x 100 cm) that gradually sloped down to a water area (100 x 100

cm; <8 cm deep). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided

that was constructed of eight lengths (80 cm long) of 10 cm (diameter) PVC pipe

strapped together in the horizontal plane and mounted on legs (5 cm). Hides were

centrally positioned in the water (partly immersed) and overhung the land.

Feeding

In both experiments, feeding occurred at 16:00-17:00 h six days a week, with waste

removed the following morning (08:00-09:00 h) when the water was changed. In the

thermal experiment, all animals were fed chopped red meat supplemented with di-

calcium phosphate (4% by weight) and a multivitamin supplement (1%). In the

feeding experiment, two groups of approximately 10-11 hatchlings were used to test

each of the four feeding treatments:

304

1. Standard mince: red meat (horse) minced through a 10 mm plate. This is the

standard diet currently provided to hatchling C. porosus in captivity (Mayer

1998; Davis 2001).

2. Short chop: red meat (horse) chopped in small pieces (8 long x 8 wide x 4 mm

thick). Prey items in the wild are captured whole and broken into pieces of

various sizes before consumption.

3. Long chop: red meat (horse) chopped in long pieces (35 long x 5 wide x 4 mm

thick). Prey items in the wild are captured whole and broken into pieces of

various sizes before consumption.

4. Variety short chop: a variety of red meat (horse), fish (white bait), prawns, pork,

and chicken meat chopped in small pieces (8 long x 8 wide x 4 mm thick).

Hatchling C. porosus in the wild consume a range of different prey types.

All four diets also contained di-calcium phosphate (4% by weight) and a multivitamin

supplement (1% by weight).

Temperature regime

In the feeding experiment, water temperature (Tw) was maintained at 31-32°C with

thermostatically controlled injection of warm water. Air temperature (Ta) varied on a

daily cycle from 26-35°C and there was a natural light cycle. In the thermal

experiment, Tw was maintained with two thermostatically controlled aquarium heaters

(200 W, Hydor Theo®

), while Ta was maintained with two thermostatically controlled

305

ceramic heaters (250 W, Oz Black URS®) positioned 40 cm above the land surface.

Temperature data-loggers (Thermocron iButtons®

) were used to measure hourly Tw,

and Ta at two sites, one at hatchling level (Ta(5)) 5 cm above the land surface, and the

other (Ta(20)) 20 cm above the land surface. In the thermal experiment, two groups of

approximately 10 hatchlings were used to test each of the four temperature treatments:

1. Constant Temperature: Tw and Ta heated constantly at 32-34ºC. This is the

standard thermal regime currently provided to hatchling C. porosus in

captivity (Mayer 1998; Davis 2001).

2. Warm Night: Tw and Ta heated during the night only (21:00-04:00 h: 7 hours

total) at 32-34ºC. While Ta increased with ambient conditions during the day,

Tw did not. This treatment provided heat at night, a time when hatchling C.

porosus are most active and use the water more frequently (Brien et al. 2012).

3. Warm Day: Tw and Ta heated during the day only (10:00-17:00 h: 7 hours

total) at 32-34ºC. This treatment provided heat during the day when hatchling

C. porosus spend the majority of time inactive under cover and prefer to

maintain a higher Tb (Brien et al. 2012).

4. Gradient: Tw not heated at all, and maintained at 28-30ºC. Ta heated constantly

at 32-34ºC. The treatment created a thermal gradient from the water (cool) to

the land (warm), providing a constant range of thermal options within the Tset.

Most reptiles housed in captivity are provided with a thermal gradient that

enables them to thermoregulate (Peaker 1969; Pough 1991).

In all four treatments, an attempt was made to maintain Ta and Tw close to the thermal

306

set point range (Tset) of Tb’s preferred by hatchling C. porosus: 29.4-32.6ºC (Brien et

al. 2012).

Behaviour


record general feeding and thermoregulatory behaviour on a digital video recorder

(Signet 4CH QV-8104). Observations were made over three days prior to recapturing of

animals at the end of the experimental period (18-20 days).


Statistical analyses were performed using JMP 8.0 statistical software (SAS Institute

Inc., 2010). Where appropriate, data were checked for normality (Shapiro-Wilk’s test)

and homoscedasticity (Cochran’s test) prior to statistical analysis. The relationship

between initial BM and Growth in BM was examined using regression analyses. An

ANOVA with pair-wise comparisons was used to examine the effect of feed treatment

(Minced, Short chop, Variety chop, Long chop) and temperature treatment (Constant,

Warm Day, Warm Night, Gradient) on growth in BM (grams), with initial BM,

replicate and clutch as factors. A significance level of P<0.05 was used for all statistical

tests.

307

Results

Feeding

The majority of feeding (70-90%) occurred during the first few hours after food was

placed in the pen (16:30-21:00 h), but a little occurred in the early morning (07:00-

08:00 h) just prior to cleaning. Most of the food (>90%) was consumed in water with

very little (<10%) consumed on land at or near where the food was provided. During

feeding the jaws were clapped together repeatedly, just under the waters’ surface,

combined with intermittent sideways shaking of the head. Both behaviours appeared to

be attempts at manoeuvring food to the back of the throat while lubricating it with

water. While swallowing, hatchlings would tilt their head up at a 45-90° angle to the

substrate.

Feeding effort, behaviour and consequences varied between treatments. In the

hatchlings fed mince, a significant amount of food was lost from the sides of the mouth

as they attempted to manoeuvre the food under the waters’ surface. Individuals fed long

chopped meat often dropped the meat, after a relatively long period (15-30 s)

attempting to manoeuvre and swallow it. After the meat was dropped, individuals rarely

attempted to recover the same piece. By way of contrast, the small chopped food

appeared easier to grasp, manoeuvre and swallow, and resulted in less waste. It was

noteworthy during cleaning that waste chopped pieces in the water (short or long

chopped) created less pollution than waste mince.

308

Initial BM had a significant effect on growth (R2=0.17; F=16.48, P<0.05), which

increased with initial BM. Growth in BM differed significantly with treatment

(F2,4=5.29, P<0.05) and was highest in the short chop treatments (red meat and

variety) which achieved similar growth, and was lowest in the long chopped treatment

(Fig. 1).

Figure 1. Mean (±SE) growth in BM of hatchlings fed standard red meat in minced,

short chopped and long chopped forms, and a variety of meats in small chopped form

(two groups in each), over 21 days. Survivorship of hatchlings is based on growth in

BM predicted by Brien et al. 2014. Red lines represent the mean (central) and standard

error (top and bottom).

Animals which failed to put on BM during the trials were largely restricted to the long

chopped (43%) and minced (32%) treatments, whereas only one individual in the short

chopped treatments (red meat and variety) lost weight (Fig. 1). Based on the survival

309

probabilities predicted from growth after 24 days post-hatch for hatchling C. porosus in

captivity (Brien et al. 2013), the number of individuals expected to survive was highest

in the short chopped treatments (Short chopped: 87%; Variety short chopped: 81%),

and lowest in the Minced (59%) and Long chopped treatments (47.7%; Fig. 1).

Temperature regime

Although the prevailing temperatures were not controlled precisely due to warmer

ambient conditions during the day, the mean hourly Ta and Tw measured over 21 days

of the experiment confirmed the temperature treatments were different (Fig. 2).

Hatchlings within the Constant, Gradient, and Warm Night treatments had access to

temperatures (Ta and Tw) within the Tset for 24 hours, while those in the Warm Day

treatment only had access to temperatures (Ta and Tw) within the Tset for 16 hours.

Figure 2. The mean water temperature (Tw), air temperature at hatchling level 5cm

above land surface (Ta(5)), and air temperature 20cm above land surface Ta(20) in each

of the four different types of temperature regimes (Constant, Warm Night, Warm Day,

310

and Gradient) over 21 days.

Hatchling C. porosus in all treatments remained inactive and under the hide-board for

the majority of the day (08:00-18:00 h: 65-80%). Activity increased at dusk (17:00-

20:00 h) as hatchlings moved from under the hide-board into open areas of land and

water, and this coincided with feeding behaviour. Throughout the evening (20:00-

05:00 h) hatchlings were more commonly observed in open areas of land and water

than during the day, while there was another peak of activity at dawn (06:00-08:00 h)

which also coincided with feeding behaviour.

Habitat use by hatchlings was similar in the Constant and Gradient treatments

(Exposed on land: 35%; Exposed in water: 15%; Under hide: 50%), but differed

slightly in the Warm Night and Warm Day treatments (On land: 30%; In water: 25%;

Under hide: 45%) with hatchlings spending more time in the water at night, especially

in the Warm Night treatment (Fig. 3).

311

Figure 3. Percentage habitat use by hatchling C. porosus over a 24 h period raised

under the same conditions at different densities with two replicates for each density.

For all hatchlings, there was no significant relationship between initial BM and growth

in BM (R2=0.010; F=0.77, P=0.38). Growth in BM was significantly lower (F2,4=5.08,

P<0.05) in the Warm Day treatment (Fig. 4).

312

Figure 4. Mean growth in BM (±SE) of hatchlings raised with four different

temperature treatments: Constant, Warm Night, Gradient, and Warm Day (two groups

in each), over 21 days. Survivorship of hatchlings is based on growth in BM predicted

by Brien et al. 2013.

Based on the survival probabilities predicted from growth after 24 days post-hatch for

hatchling C. porosus in captivity (Brien et al. 2013), the number of individuals

expected to survive was highest in the Warm night (66.5%), Constant (61.5%), and

Gradient (56.5%) treatments, and was lowest in the Warm day treatment (23.5%; Fig.

4).

313

Discussion

Feeding

Hatchling C. porosus fed a short chopped form of either red meat or a variety of meats

had higher growth rates during the first three weeks post hatching than those fed the

standard minced or long chopped forms of red meat. Hatchlings appeared to be more

efficient at consuming short chopped pieces of meat than they were at consuming either

mince, which they frequently lost in the water, or long chopped pieces, which were

dropped after some effort trying to consume.

Hatchling C. porosus in the wild typically consume small prey which they break off

into pieces that they are better able to consume (Webb et al. 1991). Therefore,

providing small ‘bite’ sized pieces of meat to hatchling C. porosus may be more

suitable for maximising feeding effort and subsequent growth under captive conditions.

However, the optimal size of these pieces is still not clear.

Physical form of the food can have a significant effect on the growth of other animals,

such as chickens (Plavnik et al. 1997; Quentin et al. 2004; Zang et al. 2009) and pigs

(Bayley and Carlson 1970). In chickens, higher growth and efficiency of gain is

achieved with a pelleted form of food rather than a mash (Plavnik et al. 1997;

Wahlström et al. 1999; Preston et al. 2000; Quentin et al. 2004), and this has been

attributed to better nutrient availability (Wahlström et al. 1999; Kilburn and Edwards

2001) and an increase in daily nutrient intake (Hamilton and Proudfoot 1995).

314

In a recent study, growth of sub-adult C. porosus in captivity was improved when

individuals were fed minced chicken heads in a sausage form compared with whole

chicken heads (Webb et al. 2013), which was explained by the reduced metabolic

costs of digesting mince (Gienger et al. 2012). Although this result appears to be in

contrast with the findings of our study, lower growth of hatchlings fed mince was

attributed to the inability of individuals to consume mince efficiently. These results

highlight the importance of feed form for optimal growth in crocodilians, which is an

area that has received little attention.

Hatchling crocodilians have traditionally been fed a minced diet of fish, poultry, pig,

or red meat, based largely upon local availability and price (Hutton and Webb 1992;

Huchzermeyer 2003). While studies with hatchling C. porosus have found higher

rates of growth on a red meat diet (Hutton and Webb 1992; Davis 2001), there also

appears to be clutch specific dietary preferences, which suggests a mixture of different

protein sources may be important for growth (Manolis et al. 1990; Hutton and Webb

1992). There may also be individual differences in dietary preference as reported

found in snakes (Burghardt 1975). However, in this study there was no significant

difference between the red meat and mixed meat diets.

Temperature regime

The temperature regime to which new born hatchling crocodilians are exposed has

long been recognised as a fundamental or overriding variable in determining rates of

315

growth (Hutton and Webb 1992; Lang 1987). As a generalisation, hatchlings need to

attain preferred body temperatures (Tb=29-33ºC), while avoiding short-term exposure

to lethal high temperatures (>38ºC) and prolonged exposure to suboptimal low

temperatures (<27ºC) (Lang 1987; Brien et al. 2012). This can be achieved technically

by controlling water temperature (Tw) and air temperature (Ta) in various ways, with

or without radiant heat sources. However, differences in preferred Tb exist both within

and between species due to clutch, body size, and incubation conditions (Lang 1987;

Webb and Cooper-Preston 1989).

In this study, hatchling C. porosus provided with a thermal regime of constant warm

temperatures (Constant: 32-34ºC), a gradient of temperatures (Gradient: 28-34ºC), or

warmer night time temperatures (Warm Night), had higher growth than hatchlings

provided with warm temperatures during the day only (Warm Day). Hatchlings in the

Warm day temperature treatment had access to temperatures within the Tset for only 16

hours of the day, compared with 24 hours a day for all other treatments. Therefore, we

attribute lower growth in the Warm day treatment to reduced access to temperatures

within the Tset that may not have allowed individuals to maximise digestion and energy

absorption.

Environmental temperatures have an important influence on the physiology, growth and

survival of ectotherms, with most species operating efficiently within an optimal range

(Pelletier et al. 1995; Rhen and Lang 1999). Lower rates of growth and survival have

been reported in abalone (Britz et al. 1997), lobster (Lellis and Russell 1990), fish

(Meeuwig et al. 2004), lizard (Waldschmidt et al. 1986), and other crocodilians (Lang

316

1987; Pina and Larreira 2002) when held under captive conditions with limited or no

access to optimal temperatures (Panov and McQueen 1998; Rhen and Lang 1999).

However, even when optimal temperatures are provided, the nature of the thermal

regime can also have a strong influence on growth and survival (Peterson and

Robichaud 1989; Dong et al. 2006).

In this study, growth of hatchling C. porosus was lowest in the fluctuating regime

(Warm Day) that best replicated the diel cycle of preferred Tbs recorded for hatchling

C. porosus in a thermal gradient (Brien et al. 2012). As with other species of reptile

(Christian 1986), hatchling C. porosus prefer cooler Tbs at night. Therefore, this

fluctuating regime, which allowed ambient conditions to drop just below the Tset over

night (28ºC), was expected to achieve similar, if not improved rates of growth in this

study. However, unlike in the wild where the availability of food is limited (Webb et al.

1991), hatchling C. porosus in captivity are provided with food every day which may

necessitate higher Tbs throughout a 24h period for digestion.

A thermal regime fluctuating or alternating on a diel cycle has been found to improve

growth and survival relative to constant temperatures in species of shrimp (Miao and

Tu 1996), sea star (Sanford 2002), and fish (Sierra et al. 1999). However, other

studies with crayfish (Thorp and Wineriter 1981), fish (Lyytikainen and Jobling

1999), and crocodiles (Kanui et al. 1991) have found no difference between a constant

and fluctuating temperature regime. While the underlying mechanism for these

different responses is unknown, it is likely related to the specific ecology of a species

and the nature of food conversion and energy allocation (Brett 1971; Diana 1984;

317

Dong et al. 2006).

Management implications

Growth and survival of ectotherms in captivity is strongly influenced by the feeding

and thermal regime provided. The results of this study suggest that growth, and thus

survival, of hatchling C. porosus in captivity can be improved by providing ‘bite’

sized pieces of meat instead of mince and a thermal regime that enables 24h access to

temperatures within the Tset for this species. However, further research is required to

establish the optimal size of the food and nature of the thermal regime.

Acknowledgements

We thank Wildlife Management International for the supply of animals, use of

facilities and logistical support. WMI funding through the Rural Industries Research

and Development Corporation is gratefully acknowledged. Funding for equipment

(cameras, digital video recorders) was provided through a Holsworth Wildlife

Research Endowment (ANZ Trustees Foundation), Northern Territory Research and

Innovation Board student grant, IUCN-SSC Crocodile Specialist Group Student

Research Assistance Scheme grant, and Charles Darwin University. Experimental

protocols were approved by the Charles Darwin University Animal Ethics Committee


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327

Chapter 5.4. Use of diazepam and tryptophan to reduce stress and

increase growth and survival of hatchling saltwater crocodiles

(Crocodylus porosus) in captivity

Abstract

In this study, 120 hatchling saltwater crocodiles (C. porosus) from four separate

clutches were divided randomly into 12 sibling only groups (N=10), with four groups

fed chopped red meat (RM), four fed chopped red meat with Valium® (VRM: 0.2-

0.8mg/kg body mass), and four fed chopped red meat with L-Tryptophan (TRM: 2%

wet weight of food). All hatchlings were raised in the same enclosures under semi-

controlled conditions for 21 days, with daily estimates of food eaten recorded and the

increase in individual body mass (g) used as an index of growth. Behaviour was

described and quantified (infrared CCTV cameras) in the evenings (17:00-08:00h) for

five consecutive nights (days 15-19). In clutch 1, hatchlings in the VRM treatment

(0.8mg/kg; -1.18±1.39 g) had significantly lower growth in BM (g) after 22 days than

those from either the TRM (2% wet weight; 13.05±4.82 g) or RM (25.29±3.8 g)

groups and this was reflected in the amount of food eaten. The mean number of

agonistic interactions observed per night (days 15-19; 17:00-08:00h) was lowest in the

VRM group (1.0±0.32 per night) compared to the TRM group (10.2±1.32 per night;

P<0.05) and RM group (15.0±1.61 per night; P<0.05). Based on lower growth and

food consumption observed in the VRM group from clutch 1, it was decided to lower

the dosage of valium provided to the VRM groups in clutches 2-4 to 0.2mg/kg.

However, after 10 days, the trend in food consumption in the VRM groups (clutches

2-4) appeared similar to that observed in clutch 1 at the higher dosage (0.8mg/kg).

328

Due to welfare concerns, experimental treatments were discontinued at day 10, with

all hatchlings fed RM until 22 days post-hatching. Differences between treatments in

growth, food consumption after 21 days and the frequency of agonistic behaviour

(days 7-9) in clutches 2-4 followed a similar pattern to that observed in clutch 1. The

results of this study suggest that while the provision of Valium® in the food may

reduce the frequency of agonistic interactions among hatchling C. porosus it can also

lead to reduced growth at dosages between 0.2-0.8mg/kg body mass.

Introduction

Stress in animals can be caused by a wide range of stimuli and conditions, causing an

elevation in the glucocortiod hormone, corticosterone, which has important

behavioural and physiological implications for survival (Romero and Wikelski 2001;

Overli et al. 2002). Prolonged or chronic elevation in corticosterone due to stress can

result in decreased growth, lower activity, and a depressed immune system relative to

conspecifics (Overli et al. 1999; 2002). Animals in production situations are

particularly susceptible to high levels of stress through social aggression and the

nature of the captive-rearing environment itself (Boissy 1995; Andersen et al. 2000;

Forkman et al. 2007).

Lower rates of growth and survival correlated with high levels of corticosterone have

been reported in hatchling and juvenile crocodilians under farm conditions (Elsey et

al. 1990; Turton et al. 1997; Isberg et al. 2009). For hatchling C. porosus, this is

known as ‘failure to thrive syndrome (FTT)’ or ‘runtism’ (Mayer 1998; Isberg et al.

329

2009; Brien et al. 2014). For reasons that are not clear, 15-40% of C. porosus

hatchlings eat and grow little relative to others, including siblings, and become

vulnerable to mortality through reduced immunity to disease or voluntary starvation

or both (Onions 1987; Mayer 1998; Isberg et al. 2009). These individuals typically

have high levels of corticosterone and usually die between 70-200 days, or need to be

culled for both efficient production and welfare considerations (Turton et al. 1997;

Huchzermeyer 2003; Isberg et al. 2009).

The saltwater crocodile has long been regarded as a species least tolerant of

conspecifics (Lang 1987; Brien et al. 2013a). Studies of agonistic behaviour in

hatchlings have revealed that social aggression among C. porosus occurs immediately

after hatching and involves actual fighting (Brien et al. 2013a). Furthermore, the

amount of growth within the first few weeks post-hatching can determine future rates

of growth and survival (Brien et al. 2014). Therefore, it is possible that social

aggression among hatchling C. porosus may promote fast growth rates in dominant

animals, and be responsible for FTT in submissive individuals.

Diazepam (Valium®) is a powerful anxiolytic benzodiazepine which is used as a

muscle-relaxant, sedative, and anti-convulsant in humans and animals (Jarvik 1970;

Andersen et al. 2000, Plumb 2002), while tryptophan is an essential amino acid, found

in most protein-based foods that can increase production of the calming

neurotransmitter serotonin (5-HT) and nictotinic acid in the central nervous system

(Grimmett and Silence 2005).

330

Diazepam and tryptophan have both been used successfully to treat aggression, fear

and anxiety in a number of animal species (rats, horses, goats, fish, and chickens)

under production conditions (Wise and Dawson 1974; Brown et al. 1976; Anika 1985;

Wongwitdecha and Marsden 1996; Warner et al. 1998; DeNapoli et al. 2000; Janczak

et al. 2001; Winberg et al. 2001; Hoglund et al. 2005). Diazepam has also been found

to increase food consumption in rats (Wise and Dawson 1974), and pigs (Dantzer

1978), while tryptophan increased food consumption in chickens (Laycock and Ball

1990). Diazepam has been used extensively as a premedicant and mild sedative in

various species of animals, establishing the safety of this drug in a wide variety of

species and resulting in established dosage ranges for various reptile species,

including crocodilians (Lloyd 1999, Schumacher and Yelen 2006).

In this study we examined the effect of diazepam and tryptophan on hatchling C.

porosus under captive conditions in reducing aggression and ultimately improving

growth and survival in the early post-hatching period. It is anticipated that if these

treatments are efficacious at reducing stress and aggression in the first few weeks

post-hatching, the resultant improved learned adaptation and adjustment to the captive

environment while on the treatment will continue once the crocodiles are weaned off

of them.

Methods

Animals and housing

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In February and March of 2012, 120 captive-born hatchling saltwater crocodiles (C.

porosus) were obtained from Wildlife Management International (WMI; Darwin,

Australia). They originated from 4 clutches collected from the wild (10-20 days old)

that had been artificially incubated at 32ºC and 95-100% humidity. After hatching

(clutch 1: 1st February; clutches 2-4: 24th February 2012), individuals remained in the

incubator (32ºC) for 3 days, which allows early detection of compromised individuals

(none found here). After three days in the incubator, 30 hatchlings from each of the

four clutches (N = 120) were divided into twelve groups of 10, each group housed

separately and consisting of ten individuals from the same clutch. For each animal,

snout-vent length (SVL - mm), and body mass (BM - g) were measured and a

uniquely numbered metal tag (Small animal tag 1005-3, National Band and Tag Co.)

was attached between the webbing on the rear right foot prior to release into the

enclosures (clutch 1: 4th February; clutches 2-4: 27th

February).

Enclosures were box shaped (170x100x50cm high) and constructed of fiberglass with

a land area (70x100cm) that gradually sloped down to a water area (100x100cm;

<8cm deep). A ‘hide area’ (Riese 1991; Mayer 1998; Davis 2001) was provided that

was constructed of eight lengths (80cm long) of 10cm (diameter) PVC pipe strapped

together in the horizontal plane and mounted on legs (5cm). Hides were centrally

positioned in the water (partly immersed) and overhung the land. Water temperature

(Tw) was maintained at 31-32°C with thermostatically controlled injection of warm

water. Air temperature (Ta) averaged around 32-34°C but varied from 26-36°C at

different times of the day depending on ambient temperatures.

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Treatment groups

All hatchling groups were fed chopped red meat supplemented with di-calcium

phosphate (4%) at 16:00-17:00 h each day ad libitum with waste removed the

following morning (08:00-09:00 h) when the water was changed. However, of the

twelve groups, four were fed just chopped red meat (RM), four were fed chopped red

meat with Diazepam (Valium®: oral form) mixed through (VRM), and four were fed

chopped red meat with tryptophan (L-Tryptophan reagent grade: Sigma-Aldrich,

USA) mixed through (TRM). Food was placed on the land and the amount left over

the next day was weighed and recorded for each group as a crude estimate of feeding

rate. Uneaten food in the water was not accounted for.

In the VRM treatment, 0.8mg/kg body mass (clutch 1) of valium was mixed in the

food. The treatment of the early clutch (clutch 1) with 0.8mg/kg of valium was

undertaken as a trial to enable improvement and refinement for the following clutches

(2-4). These dosages of diazepam are remarkably consistent among animals of various

taxa and of a wide range in body sizes, from small mammals to birds and large adult

crocodilians (Plumb 2002, Lloyd 1999). The selected range for this study was based

on a range of 0.5-2.0 mg/kg body mass used for mild sedation/calming pre-

anaesthesia in a wide variety of reptiles, including snakes and lizards, which are of a

similar body size to hatchling crocodiles (and thus likely similar in terms of metabolic

scaling of drug dosages) (Schumacher and Yelen 2006).

Diazepam has low toxicity and a relative lack of side-effects (Baldwin et al. 1990,

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Plumb 2002), and is currently approved for use with Crocodylus porosus as a sedative

according to the ‘Code of Practice on the Humane Treatment of Wild and Farmed

Australian Crocodiles 2009’ (pp. 11. section 60, 71). However, dosage rates used

were lower than what is required for sedation. The half-life for diazepam in small

animals ranges from a few to several hours, therefore if mild sedation occurs, the

effect should wear in less than a day (Plumb 2002). The reversal agent (Flumazenil -

Anexate) was on hand to be administered in case severe sedation or any other adverse

signs occur (eg. muscle fasciculations, excitement).

In the TRM treatment, tryptophan was mixed in with the standard diet at 2% of wet

mass, in accordance with previous studies (Laycock and Ball 1990; Winberg et al.

2001; Hoglund et al. 2005). Tryptophan is readily available for use by humans and

animals. No adverse side effects have been substantiated in humans or animals from

long-term use and sudden withdrawal of relatively high tryptophan from the feed has

not been noted as having adverse consequences (Leathwood 1987; Laycock and Ball

1990; Bellisle et al. 1998).

Hatchlings remained in these treatment groups for 21 days, before recapture and

measurement on day 22 (clutch 1: 26th

February 2012; clutches 2-4: 20th

March 2012),

with increase in body mass (g) for each individual used as an index of growth. Food

was withheld for 24 h prior to the second BM measurements. This time period was

selected because absolute growth of C. porosus after 24 days post-hatching in

captivity is crucial in determining future rates of growth and survival (Hutton and

Webb 1992; Brien et al. 2014). Following the experiment, all animals were returned

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to regular raising facilities where both their behavior and food consumption was

monitored for the next two weeks to ensure no ill effect of the treatments. At the

conclusion of the experiment, in order to minimize any potential withdrawal

symptoms from abrupt cessation of the diazepam, the oral treatment was administered

at one-half the dosage for a week, then at one-half the dosage on every other day for a

week prior to cessation.

Behavior


record the total number of agonistic interactions on a digital video recorder (Signet

4CH QV-8104) over a five day period (days 15-19) between the hours of 17:00-

08:00h. This time period is when the majority of agonistic interactions among

hatchling C. porosus occur under captive conditions (Brien et al. 2012; 2013a). An

agonistic interaction was defined as any interaction between individuals in which

intolerance was signaled by postures or actions by one or both individuals (Brien et al.

2013a).



Institute Inc. 2010). Where appropriate, data were checked for normality (Shapiro-

Wilk’s test) and homoscedasticity (Cochran’s test) prior to statistical analysis. To

examine differences in growth in BM (g) between treatment groups, a t-test was used

335

or a Welch’s t-test when variances were unequal. To examine differences in the

frequency of agonistic interactions between treatment groups, a Kruskal Wallis test

with Wilcoxon pair wise comparisons was used to account for small sample sizes. A

significance level of P<0.05 was used for all statistical tests. All means are reported ±

one standard error (SE).

Results

In clutch 1, hatchlings in the VRM treatment (-1.18±1.39 g) had significantly lower

growth in BM (g) after 22 days than those from either the TRM (13.05±4.82 g;

Welch’s t-test: t=2.84, df=18, P<0.05) or RM (25.29±3.8 g; Welch’s t-test: t=42.35,

df=18, P=0.0001) groups (Fig. 1), which did not differ significantly from each other

(t-test: t=-1.99, df=19, P=0.06).

Figure 1. Hatchling growth in BM (grams) after 22 days for hatchling C. porosus

from clutch 1 fed chopped red meat (RM), chopped red meat with tryptophan (TRM)

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and chopped red meat with valium (VRM). Red lines indicate the mean (central) and

the standard error (top and bottom).

Differences in BM growth (grams) between each group were reflected in crude

estimates of food consumption, which was much lower in the VRM group (total

eaten: 255 g) compared with those from the TRM (total eaten: 700 g) and RM (total

eaten: 830 g) groups (Fig. 2).

Figure 2. Crude estimate of food eaten (grams) per treatment group over 22 days for

hatchling C. porosus fed chopped red meat (RM), chopped red meat with tryptophan

(TRM) and chopped red meat with valium (VRM).

Based on lower growth and food consumption observed in the VRM group from

clutch 1, it was decided to lower the dosage of valium provided to the VRM groups in

clutches 2-4 to 0.2mg/kg. However, after 10 days, the trend in food consumption in

the VRM groups (clutches 2-4) appeared similar to that observed in clutch 1 at the

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higher dosage (0.8mg/kg). Due to welfare concerns, experimental treatments were

discontinued at day 10, with all hatchlings fed RM until 22 days post-hatching (Fig.

3).

Figure 3. Crude estimate of food eaten (grams) per treatment group for a) clutch 2; b)

clutch 3; c) clutch 4, over 22 days for hatchling C. porosus fed chopped red meat (RM

- blue), chopped red meat with tryptophan (TRM - black) and chopped red meat with

valium (VRM - grey).

Growth in BM was still measured after 22 days for hatchlings in clutches 2, 3, and 4.

In all instances, growth in BM followed a similar pattern to what was observed in

clutch 1, with highest growth among those in the RM treatment, followed by TRM

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and VRM (Fig. 4). However, these differences were not significant in the majority of

cases (Table 1).

Figure 4. Hatchling growth in BM (grams) after 22 days for hatchling C. porosus

from a) clutch 2, b) clutch 3, and c) clutch 4, fed chopped red meat (RM), chopped red

meat with tryptophan (TRM) and chopped red meat with valium (VRM). Red lines

indicate the mean (central) and the standard error (top and bottom).

339

Table 1. Growth in BM (grams) differences between treatment groups for clutches 2, 3, and 4. *indicates statistical difference.

Clutch 2 Clutch 3 Clutch 4

Treatment

groups Test Result (df=18) Test Result (df=18) Test Result (df=18)

RM and TRM Welch’s t-test t=2.74, P=0.02* t-test t=-0.47, P=0.65 t-test t =-0.85, P=0.41

RM and VRM Welch’s t-test t=2.14, P=0.06 t-test t =-0.58, P=0.57 t-test t =-2.53, P=0.02*

TRM and VRM t-test t=1.47, P=0.16 t-test t = -0.12, P=0.91 t-test t =-0.66, P=0.52

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Agonistic behavior

The mean number of agonistic interactions observed per night (days 15-19; 17:00-

08:00h) differed significantly between treatment groups from clutch 1 (X2= 11.11,

df=2, P<0.05) with fewer observed in the VRM group (1.0±0.32 per night) compared

to the TRM group (10.2±1.32 per night; P<0.05) and RM group (15.0±1.61 per night;

P<0.05) which were similar (P=0.07; Fig 5).

Figure 5. Mean number of agonistic interactions observed between hatchlings from

clutch 1 in each treatment group (RM: red meat, TRM: tryptophan and red meat,

VRM: valium and red meat) over a three night period (15-19 days) between 17:00-

08:00h. Red lines indicate the mean (central) and the standard error (top and bottom).

For hatchlings in clutches 2-4, behavioral observations were undertaken over three

nights (7-9 days post hatching; 17:00-08:00 h) prior to termination of experimental

341

treatments (VRM and TRM) on day 10. While the sample sizes were too small for

accurate statistical analyses, the mean number of agonistic interactions observed per

night followed a similar pattern to those in clutch 1, with a lower number of agonistic

interactions observed among the VRM groups (Fig. 6).

Figure 6. Mean number of agonistic interactions observed between hatchlings from a)

clutch 2 b) clutch 3, and c) clutch 4 in each treatment group (RM, TRM, VRM) over a

three night period (7-9 days) between 17:00-08:00h. Red lines indicate the mean

(central) and the standard error (top and bottom).

Discussion

While the provision of valium in the food generally appeared to reduce the frequency

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of agonistic interactions among hatchling C. porosus, it did not coincide with an

increase in growth. Based on the survival probabilities predicted from growth of

hatchling C. porosus in captivity after 24 days post-hatch (Brien et al. 2014), in the

first clutch, only 25% of animals in the valium group would be expected to survive to

200 days compared with 70% in the tryptophan group and 99% in the red meat group.

While estimates of daily and overall food consumption in this study were considered

crude, they did appear to provide a general index of growth performance. Based on

these estimates, it appeared that all hatchling groups initiated feeding regardless of

treatment, and that consumption was similar across treatments for the first four days.

This suggests that hatchlings were not initially deterred by the presence of tryptophan

(powder – no smell) or valium (liquid – sweet smell) in the food. However, after 4-5

days, food consumption by hatchlings in the valium treatment groups declined, while

the other groups continued to feed.

The benefit of oral administration in the food is that it is more practical to administer

in a production system and is less stressful on hatchlings since handling is not

required. However, a significant disadvantage of the oral form is that the actual

dosage taken in by the hatchling depends on whether, and how much, the hatchling

eats. Therefore, it is possible that the more dominant individuals within the valium

groups ate more than the intended amount and were subsequently sedated. As the

frequency of agonistic interactions between hatchling C. porosus can be used as an

index of overall activity (Brien et al. 2012), the lower frequency of agonistic

interactions among hatchlings in the valium groups would support this idea.

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Food supplemented with tryptophan has been found to reduce aggression and size

heterogeneity and improve growth in pigs, poultry and fish (Grimmett and Silence

2005). While there was a general trend for groups of hatchling C. porosus fed

tryptophan in this study to engage in slightly fewer agonistic interactions than groups

fed just red meat, growth was also slightly lower.

As one of the most aggressive species of crocodilian, social aggression is considered

one of the primary causes of FTT in hatchling C. porosus raised in captivity (Isberg et

al. 2009; Brien et al. 2013a, b). However, a recent study that examined the effect of

barriers and water levels on agonistic behaviour and growth in groups (N=10) of

hatchling C. porosus found that, while the frequency and intensity of agonistic

interactions could be reduced substantially by the provision of complex visual barriers

or deeper water, it did not coincide with improved growth (Brien et al. 2014).

Fear and anxiety in animals can be caused by situations that are unpredictable,

unfamiliar, or sudden, in which individuals feel threatened, such as a predatory attack

(Boissy 1995; Andersen et al. 2000; Forkman et al. 2007). The majority of farming

practices involve handling, size-sorting, cleaning, maintenance, and culling, which

can all induce fear and anxiety (Boissy 1995; Andersen et al. 2000; Forkman et al.

2007). As a result, fear and anxiety is common for a number of species in production

situations and is associated with elevated levels of corticosterone (Boissy 1995;

Forkman et al. 2007).

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As a small ‘prey’ species that groups together, occupies sheltered habitat, and that

spends most of the time avoiding predators, hatchling C. porosus may be susceptible

to high levels of fear and anxiety in production situations (Lang 1987; Webb and

Manolis 1989). Hatchling C. porosus on farms will rapidly and consistently flee for

cover (eg. water, hide) in response to any form of disturbance (pers. obs). When

raised without any form of cover, hatchling C. porosus will pile together in the corner,

which is interpreted as a stress response, and will invariably grow poorly (Riese 1991;

Mayer 1998; Davis 2001). Therefore, FTT in hatchling C. porosus may be caused by

high levels of fear and anxiety induced by the raising environment itself, rather than

as a product of agonistic behaviour.

Acknowledgements

I would like to thank Wildlife Management International for the supply of animals,

use of facilities and logistical support. Thank you to my supervisors, Keith Christian,

Grahame Webb, Keith McGuinness, Jeff Lang, and Cathy Shilton from Berrimah

Veterinary laboratories in Darwin for their help with experimental design and edits.

WMI funding through the Rural Industries Research and Development Corporation is

gratefully acknowledged. Funding for equipment (cameras, digital video recorders)

was provided through a Holsworth Wildlife Research Endowment (ANZ Trustees

Foundation), a Northern Territory Research and Innovation Board student grant,

IUCN Crocodile Specialist Group student grant, and Charles Darwin University.



345

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Chapter 6. Improving growth and survival in hatchling C. porosus:

summary, outdoor enclosures, and conclusions

The central focus of this thesis was to examine two poorly understood aspects of

hatchling behaviour in saltwater crocodiles (Crocodylus porosus), agonistic and

thermoregulatory behaviour, and to gain insights through experimentation into the

roles they may play in various factors influencing hatchling growth and survival rates

in captive raising facilities. The majority of studies relied on the use of infrared CCTV

cameras positioned within experimental enclosures to observe behavioural

interactions, and temperature data-loggers were used to monitor body temperatures in

relation to the environment.

Agonistic behaviour

After reviewing the first video recordings, it was clear that C. porosus are born with

the repertoire of agonistic behaviours. Sixteen distinctive behaviours were described

which are similar to those observed in adults. The majority of agonistic interactions

were observed between two individuals in the morning (06:00–08:00 h) and evening

(17:00–20:00 h) in open areas of shallow water. There were clutch specific

differences in the frequency of agonistic interactions. However, ontogenetic changes

occurred, with a smaller subset of behaviours based on dominance status displayed by

13 and 40 weeks.

It was concluded that agonistic behaviour is important in establishing and maintaining

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dominance hierarchies in C. porosus, characterised by aggression–submission

interactions. This type of interaction appears typical for C. porosus both in the wild

and in captivity, and may be important in preventing serious injury in a species

equipped with formidable armoury. Dispersal by hatchling C. porosus at around 13

weeks of age appears to be driven by a growing intolerance of conspecifics, while

territoriality is apparent at an early age.

To test whether the repertoire of behaviours described in hatchling C. porosus was

ubiquitous across all crocodilians, agonistic behaviour was also examined in seven

other species of crocodilian with an initial comparison made with C. johnstoni. In

contrast with C. porosus of a similar age, agonistic interactions between C. johnstoni

were conducted with relatively low intensity, showed limited ontogenetic change, and

there was no evidence of a dominance hierarchy among hatchlings by 50 weeks of

age, when the frequency of agonistic interactions was lowest. The head was also

rarely targeted in contact movements with C. johnstoni because they exhibit a unique

‘head raised high’ posture, and engage in ‘push downs’. Agonistic interactions

between C. johnstoni and C. porosus at 40–50 weeks of age were mostly low level,

with no real exclusion or dominance observed. The nature of agonistic interactions

between the two species suggests that dominance may be governed more strongly by

size rather than species-specific aggressiveness.

Comparisons of agonistic behaviour between the seven other species of crocodilian

(Australian freshwater crocodiles (Crocodylus johnstoni), American alligators

(Alligator mississippiensis), New Guinea freshwater crocodiles (Crocodylus

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novaeguineae), Gharials (Gavialis gangeticus), Siamese crocodiles (Crocodylus

siamensis), dwarf caimans (Paleosuchus palpebrosus) and Morelet’s crocodiles

(Crocodylus moreletti), and C. porosus revealed that the nature and extent of agonistic

interactions, the behaviours displayed (3 species-specific), and the level of conspecific

tolerance varied among species. The saltwater crocodile was considered the most

aggressive species, followed by C. novaeguineae, both of which appeared to form

dominance hierarchies, whereas the less aggressive species did not. It was concluded

that interspecific differences in agonistic behaviour may reflect evolutionary

divergence associated with morphology, ecology, general life history and responses to

interspecific conflict in areas where multiple species have co-existed.

Thermal behaviour

To examine thermoregulation we force-fed hatchling C. porosus (400 mm TL and 250

g BM) small temperature data loggers (Thermocron iButtons®). Data loggers were

recovered at the end of the experiments and the temperature data collected and

analysed. As very little information existed on thermoregulation in hatchling C.

porosus, the temperature range at which they chose to operate when given the

complete range of thermal options was determined. This was undertaken in a thermal

gradient where environmental temperatures were thermostatically controlled and

maintained.

It was found that hatchling C. porosus preferred temperatures between 29.4ºC and

32.6ºC (50% of Tbs (Tset), with a mean Tb of 30.9±2.3ºC SD which was not influenced

355

by social situation (isolated, group) or whether individuals had been fed or not.

However, there was a strong daily cycle in temperature selection and activity, with

hatchlings maintaining higher Tbs during the day (11:00-17:00 h: 31.9±2.09ºC) and

moving little, compared to the evening when activity was higher and Tbs were lower

(18:00-10:00 h: 30.6±2.31ºC).

Based on the results of these earlier experiments, and previous studies involving C.

porosus, it was considered that agonistic and thermal behaviour may play a major role

in the observed differences in growth rates and survival in captivity, and as a

consequence, the high incidence of FTT in captivity. Therefore, ways of minimising

or reducing the level of agonistic behaviour and its effect on growth and survival was

investigated. The optimal thermal regime for growth and survival was also examined.

Growth and survival

Individual hatchlings have growth trajectories in body weight over time that ideally

follow a positive exponential curve, as more and more body mass accumulates per

unit length. Variation in these trajectories results in some individuals being longer and

heavier than others after the same time post-hatching time interval. It also results in

some individuals failing to thrive (FTT), losing weight, and eventually dying. A

central question addressed in this study was the degree to which individual growth, in

raising conditions considered ‘standard’ for hatchling C. porosus in the Australian

Code of Practice, could be used as indicators of later performance, and particularly of

the probability of succumbing to FTT. It was found that growth in the first 24 days

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post-hatching was a highly significant predictor of growth to 90 days and the

incidence of FTT. Hence a series of trials were undertaken testing the effects of a

range of variables considered potentially important (independent variables) in

predicting growth to 24 days of age (dependent variable).

The effect of food form (minced red meat, long- and short-chopped red meat, and a

variety of short copped meat) on initial growth at a constant temperature regime was

examined. The results determined that hatchling C. porosus fed a short chopped form

of either red meat or a variety of meats had higher growth in BM than those fed the

standard minced form or long chopped form of red meat. Hatchlings appeared to be

more efficient at consuming short chopped or ‘bite-sized’ pieces of meat than they

were at consuming either mince, which they frequently lost in the water, or long

chopped pieces, which were dropped after some effort trying to consume.

Understanding agonistic behaviour

Because agonistic interactions occurred between hatchlings in areas of shallow, open

water shortly after hatching, the effect of visual barriers and deeper water on the level

and nature of agonistic behaviour and growth was examined. However, while visual

barriers almost eliminated agonistic behaviour and deeper water reduced the duration,

intensity and outcome of interactions, it did not result in improved rates of growth.

The effect of density (3.3/m2, 6.7/m

2, 13.3 m

2, 20.0/m

2) on agonistic behaviour and

growth rates was investigated. It was found that as density increased above 6.7/m2,

357

growth in hatchling C. porosus began to decline as activity increased. Hatchlings at

these higher densities were more often in contact with others and were more active,

especially at night when they were observed circling the perimeter and appeared to be

searching for a way out. The frequency of agonistic interactions (mean per animal per

night) was highest at the lower densities (3.3/m2;6.7/m

2) and decreased with increased

density (13.3/m2; 20.0/m

2). At the lowest density (and group size: 5), one or two

individuals became dominant and grew large at the expense of the remaining

hatchlings.

In another attempt to reduce the level of agonistic behaviour and possibly increase

growth in hatchling C. porosus, the effect of supplementing food with Valium® (0.2-

0.8mg/kg) or L-Tryptophan (2% wet weight) was examined. While hatchlings in the

initial group fed Valium (0.8mg/kg) had a far lower frequency of agonistic

interactions compared with the control and L-Tryptophan groups, they also had the

lowest overall rate of growth. While the experiment was replicated again (4 more

groups) at a lower dosage of Valium® (0.2mg/kg), the trend in food consumption

suggested lower growth would again occur in the Valium® groups and so the decision

was made to discontinue the experiment after 10 days. The results of this study

suggest that while the provision of Valium® in the food may reduce the frequency of

agonistic interactions among hatchling C. porosus it can also lead to reduced growth

at dosages between 0.2-0.8mg/kg.

These studies were focussed on visual displays of agonistic behaviour, and there is no

doubt that this species is capable of communicating through vocal or chemical means.

358

Hatchlings were detected vocalising (ripples made in water as gular pouch fluttered)

on different occasions, which often elicited a response from one if not more

individuals in the enclosure. While this has been reported previously (Britton 2001;

Verne et al. 2012), chemical communication has received very little if any attention in

crocodilians let alone C. porosus. The presence of semio-chemical glands in the

cloaca and in the gular pouch of C. porosus, suggests that chemical communication

may play an important role and is an area of study that deserves further attention. In

any instance, it is likely that C. porosus communicate and interact through a

combination of visual, vocal, and chemical means, and that understanding this

relationship may hold the key to identifying and managing the primary causes of FTT.

Optimal thermal regime

Given the clear diurnal pattern of thermoregulation among hatchling C. porosus, the

effect of adjusting the thermal regime on initial rates of growth and survival was

examined. We created four thermal regimes within enclosures (constant: 32-34ºC,

gradient: 28-34ºC, warm night: 32-34ºC, warm day: 32-34ºC) using the results of the

earlier thermal regime study (Tb, Tset) as a guide. Hatchlings under constant warm

temperatures, a gradient of temperatures, or warmer night time temperatures, had

higher growth than hatchlings provided with warm temperatures during the day only.

This result was unexpected, given that the warm day treatment best replicated the

diurnal pattern observed in earlier studies. However, when examined in the context of

the Tset, hatchlings in the warm day temperature treatment had access to temperatures

within the Tset for only 16 h of the day, compared with 24 h a day for all other

359

treatments. Therefore, constant access to temperatures within the Tset appears to be

important for optimal growth and survival of hatchling C. porosus under captive

conditions.

It is clear that hatchling C. porosus have a range of temperatures at which they prefer

to function, and that they have a diurnal pattern of activity and thermoregulatory

behaviour. The results of our studies suggest that hatchlings under captive conditions

require constant access to this preferred range of temperatures within their

environment. However, it does not seem necessary to maintain constant air and water

temperatures, as long as a section of the environment is maintained within this range.

The raising environment: a case study

While the results of these studies have shed some light on previously unknown

aspects of thermal and agonistic behaviour in hatchling C. porosus and the influence

on growth and survival, the question of what causes FTT and how it can be reversed

or prevented remains unknown. By the end of these experiments, it was decided that

perhaps the actual raising environment itself may be contributing to the high levels of

stress experienced by hatchlings leading to FTT. Therefore, it was decided to examine

how hatchlings afflicted by FTT to varying degrees, and likely to deteriorate much

further unless provided with special care, may respond when placed into a semi-

natural enclosure as opposed to remaining in standard raising pens. Standard pens are

those described in the density experiment: comprising land and water areas, constant

warm temperatures (32ºC: air, water), hide-boards, and low densities (<15 crocodiles

360

per m2).

Methods

A total of 505 hatchling C. porosus (24-57 days old) of a similar size (332.9±0.61 mm

TL range 300-374 mm; 69.7±0.43 g BM range 47-89 g) and considered to be afflicted

by FTT were obtained from Wildlife Management International (WMI), Darwin

(Australia). Hatchling C. porosus originated from clutches of eggs collected from the

wild (2-30 days old when collected) and from captive bred stock that had been

artificially incubated at 32ºC and 95-100% humidity. All had been raised in the same

standard raising pens, with constant water temperature (32-34ºC), and air temperature

fluctuating a few degrees higher during the day (34-38ºC) than at night (17-22ºC).

On 13 April 2012, 405 hatchlings were captured and redistributed back into the

standard raising pens in three groups of 5 (2m2), 10 (4m

2), 20 (6m

2), 40 (12m

2), 60

(18m2) at a density of 2.5-3.3 crocodiles per m

2. The other 100 hatchlings were

released into a semi-natural enclosure (202m2; 0.5 crocodiles per m

2; Fig. 1) that was

designed to replicate conditions in the wild. The enclosure was largely earthen and

specifically designed to replicate conditions experienced by hatchling C. porosus in

the wild in the Northern Territory.

The enclosure was rectangular (36m long x 10m wide) and enclosed by a 1-1.5m high

wire mesh fence with bird netting over the top to prevent access by predators. It had a

centrally located channel of water (36m long x 5.6m wide x 1.3m deep) with land on

361

each side. The land on one side (36m x 3.2m) sloped down on a 40º angle (approx.),

and the other bank was flat (36m x 1.3m). Land was densely covered with grass and

small bushes, except for a section of black high density polyurethane plastic (10m x

1.3m) designed to replicate mud banks commonly found in the wild and used by

crocodiles for basking.

Figure 1. Semi-natural enclosure replicating conditions naturally occurring in the

wild.

A single uniquely numbered metal webbing tag (Small animal tag 1005-3, National

Band and Tag Co.) was attached to the rear back right foot at the time of release into

the enclosures. Body mass (BM in g) was measured when the animals were

introduced into the initial enclosures, and again after 27 days (10th

May 2012). All

hatchlings were fasted the day prior to measurements being taken. All animals were

fed chopped or minced red meat supplemented with di-calcium phosphate (4%) and a

multivitamin and mineral supplement (1%). Feeding occurred at 16:00-17:00 h each

362

day throughout the study, with food placed on the edge of the bank near the water and

the waste removed the following morning (08:00-09:00 h).


Statistical analyses were performed using JMP 8.0 statistical software (SAS Institute

Inc., 2010). Regression analyses were used to examine the relationship between initial

BM and final BM and Growth in BM. An ANOVA with Tukeys pairwise

comparisons was used to examine initial BM between groups. An ANOVA with

replicate and clutch as factors, and initial BM as a covariate was used to examine

differences between groups in final BM and growth in BM. Tukeys pairwise

comparisons were used to examine differences between individual groups.

Results

While environmental temperatures within the semi-natural enclosure fluctuated during

the day, temperatures within the standard raising pen were thermostatically controlled

and maintained at a more or less constant temperature (Fig. 2).

363

Figure 2. Environmental temperatures in the a) semi-natural enclosure: air

temperature at 1.5m, water temperature 5cm below the surface, soil surface in the

shade, soil surface in the sun; and within the b) standard raising pen: air temperature

measured at 1.5m above the ground and just above the ground at crocodile height, and

water temperature.

There was a stronger positive linear relationship between initial BM and final BM

among hatchlings in the standard raising pens (R2=0.47, F=352.14, P<0.05) compared

with those in the semi-natural enclosure (R2=0.14, F=15.49, P<0.05; Fig. 3a). While

there was also a strong linear relationship between initial BM and growth in BM in

the standard pens (R2=0.16, F=74.69, P<0.05), there was no such relationship among

hatchlings in the semi-natural enclosure (R2=0.03, F=2.65, P=0.11; Fig. 3b).

364

Figure 3. Relationship between initial BM and a) final BM and b) growth in BM of

hatchling C. porosus suspected of suffering from FTT within standard raising pens

(grey: 5, 10, 20, 40, 60), and within a semi-natural enclosure (blue: 100).

Initial BM differed significantly between groups (F3,6 = 8.75, P<0.05) and was lowest

among groups of 5, 60, and also 100: which was the semi-natural enclosure (Fig. 4a).

Final BM (F2,13 = 7.50, P<0.05) and growth in BM (F2,13 = 7.45, P<0.05) also differed

significantly between enclosure types and was highest in the group of 100 hatchlings

in the semi-natural enclosure (Fig. 4b,c).

365

Figure 4. Mean size and growth in BM (grams; ±SD and SE) of hatchling C. porosus

suspected of suffering from FTT after 27 days within standard raising pens (5, 10, 20,

40, 60), and within a semi-natural enclosure (N=100).

The number and percentage of hathlings that lost weight during the study period was

lowest in the semi-natural enclosure (100: 4%) and highest among those in the

standard raising enclosures (5: 80.0±11.6%; 10: 30.0±5.8%; 20: 51.7±11.7%; 40:

50.8±14.3%; 60: 61.1±12.3%).

366

Discussion

In this study, mean growth in BM (grams) of hatchlings in the semi-natural enclosure

was more than double that of hatchlings in the standard raising pens after 27 days.

This suggests that captive raised hatchling C. porosus suffering from FTT may benefit

from being moved into a more natural enclosure. While it is not exactly clear why this

may be the case, there are a broad range of interrelated factors that could potentially

explain this result. For instance, there was an abundance of live prey (eg. tadpoles,

fish, insects) in the semi-natural enclosure, which hatchling crocodilians are known to

instinctively chase and consume, even those afflicted by FTT (Webb et al. 1991;

Hutton and Webb 1992). It has also previously been reported that the provision of live

food to hatchling C. porosus afflicted by FTT can improve growth and survival under

captive conditions (Garnett 1986; Mayer 1998).

There was a strong positive relationship between initial BM and growth BM among

hatchlings within the standard pens. However, there was no such relationship among

hatchlings in the semi-natural enclosure. As the most aggressive and intolerant species

of crocodilian (Lang 1987), in which agonistic behaviour begins shortly after hatching

(Brien et al. 2013), hatchling C. porosus may require more space per individual and a

more complex environment to mitigate against negative social interactions. The

ability of hatchlings to avoid or escape negative social interactions would have been

far greater within the semi-natural enclosure and may have resulted in the higher

growth rates regardless of initial size.

367

The level of disturbance experienced by hatchling C. porosus was considerably lower

in the semi-natural enclosure. As part of the cleaning regime in the standard pens each

morning, all the water was drained, hide-boards were lifted, and the leftover food

hosed out. This process involved two people getting within 1m of the hatchlings, and

took up to an hour before the water was then refilled at a cooler temperature. In

comparison, the leftover food in the semi-natural enclosure was removed each

morning by one person, which took less than 10 minutes and did not require draining

of the water. During this time, hatchlings remained hidden in the dense vegetation on

the opposite bank, which was a distance of more than 5m.

As a small ‘prey’ species that groups together, occupies sheltered habitat, and that

spends most of the time avoiding predators, hatchling C. porosus may be susceptible

to high levels of fear and anxiety in production situations (Lang 1987; Webb and

Manolis 1989). Hatchling C. porosus on farms will rapidly and consistently flee for

cover (e.g. water, hide) in response to any form of disturbance (pers. obs). When

raised without any form of cover, hatchling C. porosus will pile together in the corner,

which is interpreted as a stress response, and will invariably grow poorly (Riese 1991;

Mayer 1998; Davis 2001). Hatchling C. porosus in the semi-natural enclosure were

rarely sighted and likely experienced lower levels of stress than hatchlings in the

standard pens.

Environmental temperatures in the semi-natural enclosure were high enough

throughout most of the day to enable hatchling C. porosus to maintain Tb’s within the

preferred range (Tset). Hatchling C. porosus were originally raised on commercial

368

farms in outdoor earthen enclosures (Hutton and Webb 1992). However, in many

cases, while rates of growth and survival were reportedly high during the summer,

they were comparatively very low during the winter and this was attributed to

temperatures below optimal for the species (Riese 1991; Isberg et al. 2009). This

resulted in a shift to indoor enclosures where environmental temperatures were

constant and warm (30-33ºC), which resulted in improved rates of growth and

survival (Webb and Manolis 1990; Hutton and Webb 1992). However, rates of FTT

affliction remained high.

Conclusions and Recommendations

The possibility that the current ‘indoor’ raising paradigm for hatchling C. porosus,

instigated some 30 years ago based on the alligator model (Hutton and Webb 1992), is

fundamentally compromised cannot be rejected. While it was initially considered that

‘outdoor’ enclosures would provide a more natural and suitable raising environment

(Hutton and Webb 1992), it seems that the inability to efficiently overcome lower

winter temperatures may have led to the abandonment of outdoor enclosures

altogether. However, in doing so the ‘baby may have been thrown out with the bath

water’.

Based on these results, it could be argued that raising hatchling C. porosus in outdoor

enclosures may lead to improved rates of growth and survival as long as

environmental temperatures can be maintained within the Tset throughout the year.

This could be achieved by covering sections of the enclosure which may provide

369

hatchlings with a range of thermal options within the Tset. This has been achieved with

juvenile Nile crocodiles (Huchzermeyer 2003) and may enable higher rates of growth

and survival throughout the year. In any case, future studies involving C. porosus may

benefit from experimentation in outdoor enclosures.

Acknowledgements

I thank Jemeema Brien and Charlie Manolis for their help in different phases of the


supply of animals, use of facilities, logistical support and major funding for this

project. WMI funding through the Rural Industries Research and Development

Corporation is gratefully acknowledged. Funding was provided through a Holsworth

Wildlife Research Endowment (ANZ Trustees Foundation), Northern Territory

Research and Innovation Board student grant, and Charles Darwin University.



Literature Cited

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NSW: Surrey Beatty and Sons. pp. 364-377.




Garnett, S.T., and Murray, R.M. 1986. Factors effecting the growth of the estuarine


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porosus in commercial crocodile farming. M.Sc thesis, University of Queensland.


Verne, A.L., Aubin, T., Martin, S., and Mathevon, N. 2012. Acoustic communication

in crocodilians: information encoding and species specificity of juvenile calls. Animal

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Webb, G.J.W., and Manolis, S.C. 1990. Raising C. porosus hatchlings in a controlled






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I have learned that the line between success and failure is often very thin and comes

down, not so much to skill or intelligence, but to what extent you are willing to stick it

out even when things get tough.

growth and survival of hatchling saltwater crocodiles (crocodylus porosus…44878/thesis_cdu... ·...

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