21

Seed Dispersal Effectiveness of Rhesus Macaques

In Chapter 2, I examine the main question of my dissertation – the role of a common

species, the rhesus macaque, as seed dispersers in the forests of northern India. Due

to their large group sizes, home ranges and daily path lengths, occasional high

percentage of fruit in the diet, and ecological resilience, I predicted that rhesus

macaques may potentially be effective seed dispersers in disturbed forests. To test my

prediction I examined seed dispersal effectiveness in rhesus macaques using the SDE

(Seed Disperser Effectiveness, Schupp, 1993; modified to Seed Dispersal Effectiveness,

Schupp et al., 2010) framework which comprises qualitative and quantitative aspects.

More specifically, I studied (i) the number of fruit species dispersed by rhesus

macaques, (ii) macaque seed handling methods, (iii) their rates of seed predation and

(iv) germination and establishment rates of dispersed seeds.

22

Chapter 2

Seed Dispersal Effectiveness of Rhesus Macaques*

Abstract

Frugivorous primates are important seed dispersers and their absence from forest

patches is predicted to be detrimental to tropical forest regeneration and recruitment.

With the reduction of primate populations globally, ecologically-resilient common

primate species, characterized by dietary flexibility and the ability to thrive in a

variety of habitats, assume new importance as seed dispersers. The most widely

distributed non-human primate, the rhesus macaque Macaca mulatta, has been

intensively studied but little is known about its role in maintaining ecosystem

structure and functions. Due to their frugivorous diet, large group sizes, large home

ranges and tolerance to disturbance, rhesus macaques may be effective seed

dispersers. To test this hypothesis, I studied seed dispersal by rhesus macaques at the

Buxa Tiger Reserve, India, through a combination of behavioural observations and

germination experiments. Rhesus macaques dispersed 84 % of the 49 species they fed

on either through spitting or defecation. Nearly 96 % of the handled seeds were

undamaged and 61% of the species for which germination tests were performed had

enhanced germination. Almost 50 % of the monitored seeds among those deposited

in situ germinated and 22 % established seedlings, suggesting that rhesus macaques

are important seed dispersers in tropical forests. Due to their widespread distribution

and large populations, rhesus macaques are perceived as common and are categorized

as Least Concern on the IUCN Red List, effectively excluding them from any

conservation plans. Based on the results of my study, I argue that rhesus macaques

fulfill critical ecological functions in their habitat and that this parameter must be

taken into consideration when they are reviewed for conservation priorities.

*A version of this Chapter has been published: Sengupta, A., McConkey, K.R. & Radhakrishna, S. (2014)

Seed dispersal by rhesus macaques Macaca mulatta in northern India. American Journal of Primatology,

76, 1175-1184.

23

2.1 Introduction

As seed dispersers, frugivorous primates are ecologically critical species (Garber &

Lambert, 1998; Chapman & Russo, 2007) and their absence from forest patches is

predicted to lead to lowered rates of tropical forest regeneration and recruitment,

thereby altering plant community structure (Anzures-Dadda et al., 2011). Land use

changes involving forest transformations have led to the loss of large numbers of

primate populations globally (Anzures-Dadda et al., 2011). In such a scenario, the

importance of ecologically-resilient primate species, characterized by dietary

flexibility and ability to thrive in a variety of habitats, increases manifold (Albert et al.,

2014). It has, in fact, been suggested that in many parts of tropical and subtropical

Asia, where forests are fragmented or native mammal fauna has gone extinct,

disturbance-tolerant macaques like the rhesus macaque Macaca mulatta, the bonnet

macaque M. radiata and the long-tailed macaque M. fascicularis may be the only seed

dispersers, especially for the large fruit/seed bearing species (Lucas & Corlett, 1998).

Hence extirpation or even a decline in the number of these macaques would

negatively impact seed dispersal in such areas (Lucas & Corlett, 1998).

Rhesus macaques have the largest geographical distribution among non-

human primates with their range spanning Afghanistan, Bangladesh, Bhutan, India,

Nepal, Pakistan, China, Burma, Laos, Thailand, and Vietnam (Fooden, 2000; Brandon-

Jones et al., 2004;). Highly adaptable, often commensal and classified as ‘Least

Concern’ on the IUCN Red List (IUCN, 2015), M. mulatta has been intensively studied

both in the field as well as laboratory (Richard et al., 1989). Yet little is known about

its role in maintaining ecosystem structure and functions. Although highly flexible in

their feeding ecology, fruits may constitute as much as 70 % (Fooden, 2000) of rhesus

macaque diet. Being semi-terrestrial, they can also include fruits of species at different

strata of the forest (Albert et al., 2013). Their large group sizes (mean: 40, Richter et al.,

2013) mean that a large number of individuals can feed on a patch at the same time

thereby dispersing considerable amounts of seeds at a time (sensu Albert et al., 2013).

Their large home (mean: 593.3 ha, Makwana, 1978) and daily ranges (mean: 1803 m,

Makwana, 1978) imply that individuals can carry seeds to large distances from the

parent trees (Albert et al., 2013). Finally, because of their ability to thrive in a range of

habitats (including fragmented and disturbed habitats) these macaques are

ecologically highly resilient (Albert et al., 2014). These characteristics suggest that

rhesus macaques can be highly effective seed dispersers in disturbed areas. However,

available information on the effectiveness of rhesus macaques as seed dispersal agents

24

is fragmentary (Dudgeon & Corlett, 1994; Lucas & Corlett, 1998) or limited to some

aspects (Tsuji et al., 2013).

Since its conception in 1993, Schupp’s SDE (initially Seed Disperser

Effectiveness; modified to Seed Dispersal Effectiveness - Schupp et al., 2010)

framework for assessing seed dispersal activities has been seminal in this field of

research. Defined as the ‘number of new adults produced by the dispersal activities of

a disperser, SDE considers the quantitative aspect of seed dispersal (measured as the

product of number of visits made to a tree and the number of seeds dispersed per

visit) as well as the qualitative (measured as the product of the probability of seed

survival in a viable condition post-handling and the probability of the survival and

germination of the dispersed seed and the subsequent production of an adult tree)

(Schupp, 1993; Schupp et al., 2010). The most common variables examined with regard

to assessment of SDE are seed handling behaviour, dispersal distance and handling

effects on germination (Schupp et al., 2010). In terms of seed handling mechanisms,

primate species are categorised as “seed swallowers”, “seed spitters” or “seed

destroyers” (Corlett & Lucas, 1990). While spat out seeds are usually deposited singly

on the forest floor, swallowed (and defecated) seeds mostly have a clumped pattern

of deposition (Chapman, 1995). Suitable dispersal distance is a key component for

effective dispersal; not only should seeds be deposited in an area suitable for

germination, an effective disperser should also carry seeds away from the parent tree

to escape mortality due to distance and density dependent predators, pathogens and

herbivores targeting the adult (Janzen, 1970; Connell, 1971; Howe & Smallwood,

1982). Handled seeds should also be in viable condition for a disperser to be called

effective (Schupp et al., 2010). Mechanical and/or chemical scarification of seed coat in

the gut, separation of seeds from pulp and the presence of fecal matter surrounding

the seeds can all have positive implications for the germination of swallowed and

defecated seeds (Traveset & Verdú, 2002).

The aim of this Chapter was to examine the role of rhesus macaques as seed

dispersers taking into account the aforementioned aspects of SDE. More specifically,

I addressed the following questions: (i) How many plant species are dispersed by

rhesus macaques? (ii) How are the various seeds handled? (iii) How far from the

parent tree are seeds deposited? (iv) What is the effect of seed handling on

germination? and (v) What percentage of seeds deposited on the forest floor achieve

establishment?

25

2.2 Methods

2.2.1 Seed handling mechanisms and dispersal distance

I followed the macaques of Troop C from their waking site to their sleeping tree for 10

days each month (12 hours a day; 5 days each in the 2nd and 3rd weeks of each month)

and recorded feeding activity using a 30-minute interval scan sampling method

(Altmann, 1974). In each sample, I scanned the troop for 15 minutes and noted the first

item (plant species and part thereof- fruit, leaf, shoot, flower; insects; fungi) consumed

by each individual. When macaques fed upon fruits, I employed 30 minute-long focal

sampling (Altmann, 1974) on any randomly chosen adult individual to make detailed

observations on the part of the fruit consumed (whole fruit, pulp, seed) and the way

seeds were handled. I checked fruits to determine the state of ripeness (ripe/unripe)

and classified seed handling mechanisms as follows: swallowed (when the entire fruit

was ingested, digested and the seeds egested intact), spat out (when the fruit was taken

into the mouth, mostly stored in cheek pouches, cleaned of the pulp and the seeds

expectorated), dropped (when portions of fruits, e.g. epicarp, were fed upon and then

discarded) and destroyed (when seeds were consistently crunched by macaques or if

the fruits of those species were consumed in an unripe state – Kunz & Linsenmair,

2008; Albert et al., 2013).

I studied remnants of fruits/seeds beneath the feeding tree to confirm the exact

part fed upon and recorded if the macaques spat out any seed during movement

between trees. Often, a number of macaques fed upon fruits of the same tree and spat

out the seeds. As it was difficult to distinguish seeds handled by different individuals

in such conditions, I divided the number of spat out seeds found under a feeding tree

immediately after a feeding event by the total number of macaques on the tree to

obtain data on dispersal through seed-spitting. I opportunistically collected fresh fecal

material from focal individuals and examined it to check the number and status

(intact/crunched) of seeds within. I measured spat out seeds and those found in fecal

samples using calipers and assigned them to the following size categories according

to their length: small (≤ 5 mm in length), medium (> 5 mm but < 10 mm) and large (≥ 10

mm) (Chapman et al., 2010; Albert et al., 2013). Species whose seeds were observed to

be spat out just once or were found only in one fecal sample (N = 2) were not

considered for the analysis.

I recorded the locations of all fecal samples and feeding trees with a hand held

GPS unit. Additionally, every month, for a period of two days, I revisited the feeding

trees and marked conspecifics within 50 m of their canopies along four 10 m wide

26

transects radiating east, west, north and south from the tree bases. Upon identification

of a particular seed species within a fecal sample, I measured straight line distances

between the location of the fecal sample and all marked conspecifics of that tree

species. I considered dispersal distance of fecal seeds as the linear distance between

the defecated seed and the nearest (based on shortest straight line distance) tree of the

same species (McConkey, 2000) and dispersal distances of spat out seeds as the

straight line distance between the actual feeding tree and the seed deposition site

(Albert et al., 2013). Dispersal distances were estimated only for those species which

were found in at least 30 fecal samples or 30 clumps of spat out seeds. For these

analyses, I only used seeds which I had directly observed being spat out or being

egested via fecal matter.

2.2.2. Seed collection and germination experiments

In order to test the effect of rhesus macaque seed handling mechanisms on seed

germination, I collected spat out and defecated seeds from different fecal samples/spat

out clumps and different locations and sowed them along with seeds (cleaned of the

pulp) collected from intact fruits (control seeds) in a shaded nursery under similar

conditions. For Ficus species and Anthocephalus chinensis, groups of 50 seeds were

placed on moist tissue papers on petri dishes (McConkey, 2000). I monitored sown

seeds every day and watered them at an interval of 4 days during the wet months

(April to October) and at an interval of 2 days during the dry months (November to

March). I sowed a total of 1020 treated and 980 control seeds and recorded the percent

of seeds that germinated (emergence of radicle). The germination percent of control

and treated seeds and their latency periods were compared using Chi-square and

Mann-Whitney U test respectively (Zar, 2010).

I conducted in situ germination tests for spat-out seeds of 8 species (Artocarpus

chaplasha, Chisocheton paniculatus, Careya arborea, Elaeocarpus varuna, Populus gamblei,

Premna benghalensis, Cissus elongata, Syzygium formosa) and defecated seeds of 3 species

(Elaeocarpus varuna, Populus gamblei, Premna benghalensis). The choice of these species

was determined by (i) the ease of recognizing their seeds on the forest floor, and (ii)

the timing of the fruiting period that allowed us to monitor them for at least 9 months.

I inserted small pegs with identifying tapes on the ground next to the seeds and

monitored a total of 603 seeds (280 fecal, 323 spat out) to note seed germination and

seedling establishment (defined as the stage when the emerged seedling is no longer

attached to the seed and its root is firmly in the soil, Balcomb & Chapman, 2003).

2.3 Results

27

2.3.1 Seed handling and dispersal

I collected a total of 2865 scans (total observation time = 716.25 h) and 600 focal animal

samples (total observation time = 300 h) on macaque behaviour. Individuals spent 58

% of their active time on feeding. Fruits comprised 79 % of the diet (percent of diet

scans), and the macaques fed on the fruits of 49 species (seed species henceforth)

(Table 2.1). The most common seed handling mechanism was spitting; significantly

more seed species were spat out (53.1 %) than were swallowed (20.4 %), dropped (4.1

%) or destroyed (12.2 %) (χ2 = 75.3, df = 4, p < 0.001) (Fig. 2.1, Table 2.1). Seeds of four

species were both spat out and defecated (Fig. 2.1, Table 2.1), and seeds of five species

were destroyed: Acacia auriculiformis, Acacia pennata, Delonix regia, Michelia champaka,

Quercus lancaefolia and an unidentified liana species (Liana species 1).

Figure 2.1 Seed fate of species fed upon by rhesus macaques (N = 49 species)

Eighty-seven percent of fecal samples (N = 311) contained seeds and comprised

nine small-seeded (71150 seeds) and two medium-sized species (235 seeds). The mean

number of small seeds/fecal sample was 317.63 ± SD 46.95 (N = 224, range: 148-778) and

the mean number of medium seeds/fecal sample was 5.10 ± SD 10 (N = 46, range: 1-

63); the number of fecal samples containing small seeds was significantly more than

those with medium seeds (χ2 = 116.03, df = 1, p < 0.001). Seeds of all sizes were spat

out but the number of observations involving large seeds (n = 678; 20 species, 11450

seeds) was significantly greater than those involving medium (n = 68; 2 species, 2448

seeds) or small seeds (n=135; 4 species, 10403 seeds) (χ2 = 762.13, df = 2, p < 0.001). The

mean number of spat out seeds/ individual was 8.56 ± SD 1.4 for small seeds (range: 6

- 13), 6 ± SD 2.24 for medium seeds (range: 3 - 8), and 3.4 ± SD 1.3 for large seeds (range:

0

10

20

30

40

50

60

Per

ceta

ng

e o

f se

ed

sp

ecie

s

Seed Fate

28

2 - 6). None of the fecal seeds had any visible damage, while 82.5 % of the spat out

seeds were found to be intact.

Table 2.1 Seed fate of species fed upon by rhesus macaques (Troop C)

Species Family Spat out Swallowed Destroyed

Acacia auriculiformis Fabaceae x

Acacia pennata Fabaceae x

Amoora rohituka Meliaceae x

Anogeissus latifolia Combretaceae x

Anthocephalus chinensis Rubiaceae x

Antidesma diandrum Euphorbiaceae x

Artocarpus chaplasha Moraceae x

Baccauria sapida Euphorbiaceae x

Beilschmedia

gammieana

Lauraceae x

Bridelia retusa Euphorbiaceae x

Careya arborea Lecythidaceae x

Casearia spp. Flacourtiaceae x x

Chisocheton paniculatus Meliaceae x

Cissus elongata Vitaceae x x

Crataeva unilocularis Capparaceae x

Delonix regia Fabaceae x

Elaeocarpus aristatus Elaeocarpaceae x

Elaeocarpus floribundus Elaeocarpaceae x

Elaeocarpus varuna Elaeocarpaceae x x

Emblica officinalis Phyllanthaceae x

Eurya acuminata Theaceae x

Ficus benghalensis Moraceae x

Ficus benjamina Moraceae x

Ficus racemosa Moraceae x

Ficus spp. Moraceae x

Gmelina arborea Verbeneceae x

Leea spp. Leeaceae x

Mangifera indica Anacardiaceae x

Mangifera sylvatica Anacardiaceae x

Michelia champaka Magnoliaceae x

Populus gamblei Salicaceae x x

29

Polyalthia simiarum Annonaceae x

Premna benghalensis Verbeneceae x x

Quercus lancaefolia Fagaceae x

Spondias mangifera Anacardiaceae x

Syzygium cumini Myrtaceae x

Syzygium formosa Myrtaceae x

Talauma hodgsonii Magnoliaceae x

Zanthoxylum budrunga Rutaceae x

Ziziphus mauritiana Rhamnaceae x

Liana species 1* x

Liana species 2* x

Liana species 3* x

Liana species 4* x

Liana species 5* x

Liana species 6* x

Liana species 7* x * These species were identified by their vernacular (Bengali/Nepali) names

2.3.2 Dispersal distance

Dispersal distances of fecal seeds (mean = 116.5 ± SD 78.60 m, range: 29.3-774.0 m, n =

370) were significantly greater than those of spat out seeds (mean = 19.2 ± SD 7.85 m,

range: 4.9-69.0 m, n = 174; t = 22, df = 542, p < 0.001; Table 2.2). About 39 % of spat out

seeds were found within the canopy radii of the feeding trees; none of the fecal seeds

were found within the canopy radii.

Table 2.2 Dispersal distances in study area

Treatment Species (N = no. of seeds,

each collected from different

dispersal events )

Mean distance

(m)

Maximum

distance (m)

Fecal Anthocephalus chinensis (34) 64.1 84.4

Eurya acuminata (31) 69.7 90.9

Ficus benghalensis (31) 73.2 144.3

Ficus benjamina (32) 76.4 96.8

Ficus spp.(32) 73.7 103

Liana 7 (37) 91.1 126.3

Leea spp. (32) 98.6 103.6

Premna benghalensis (36) 126.6 158.7

Populus gamblei (34) 132.1 163.2

Cissus elongata (37) 160.6 226.1

30

Elaeocarpus varuna (34) 299 774

Spat Spondias mangifera (38) 15.6 22.6

Polyalthia simiarum (35) 16.6 25.7

Liana 2 (32) 16.8 23.7

Chisocheton paniculatus (35) 18.7 28.7

Syzygium formosa (33) 27.4 43.7

Artocarpus chaplasha (37) 41.9 58.1

Careya arborea (31) 42.3 56.2

Populus gamblei (32) 51.6 79.7

2.3.3. Germination trials

I obtained germination data for 68.2 % of the 2000 seeds sowed; 637 seeds were either

damaged by insects or desiccated. Of the 18 species that germinated, 12 species

showed significant differences either in the germination percent or in the latency

period of the treated seeds (Table 2.3). For Populus gamblei, although none of the

control or the spat-out seeds germinated, all the fecal seeds germinated. Premna

benghalensis and Talauma hodgsonii were two other species where only the treated seeds

germinated. For Anthocephalus chinensis, the germination percent of fecal seeds was

significantly lower than control seeds. However, the mean latency period of fecal

seeds was significantly lower than control seeds.

Table 2.3 Germination percent and latency period of treated and control seeds

Species Treatment Germination percent Mean Latency period

(days)

Control (N) Treated (N) Control Treated

Anthocephalus

chinensis

Fecal 40 (50) 20* (50) 150 50***

Artocarpus chaplasha Spat 83.3 (30) 80 (30) 33.4 34.4

Careya arborea Spat 100 (35) 100 (35) 30 17.75

Chisocheton paniculatus Spat 100 (37) 85.7 (37) 54.9 66.5

Cissus elongata Fecal 69 (34) 61 (34) 65 48

Elaeocarpus varuna Spat 100 (30) 87 (30) 48 40

Fecal 100 (30) 92.5 (30) 34 39

Ficus benghalensis Fecal 90 (50) 95 (50) 40 13***

Ficus benjamina Fecal 90 (50) 83 (50) 43 20.5**

31

Ficus spp. 1 Fecal 85 (50) 95 (50) 32 15*

Populus gamblei Spat 0 (30) 0 (30) − −

Fecal 0 (30) 50*** (30) − 41

Polyalthia simiarum Spat 30.2 (35) 46.6 (35) 173 163

Premna benghalensis Fecal 0 (30) 16.7*** (30) - 46

Spat 0 (30) 50*** (30) - 46

Spondias mangifera Spat 53 (38) 43.3 (38) 174 167

Syzygium cumini Spat 98 (30) 93.2 (30) 36 15**

Syzygium formosa Spat 100 (30) 87.2 (30) 30.1 11**

Talauma hodgsonii Spat 0 (34) 33*** (39) − 92.67

Liana spp. 2 Spat 28.6 (37) 57.1** (38) 107 76.75*

Liana spp. 3 Spat 66.7 (36) 54.5 (31) 65 33**

*P < 0.05 **P < 0.01***P < 0.001

In the case of in situ germination, at the end of the study period, 50% of the

seeds had germinated and 20 % of the seeds had disappeared (all fecal); the remaining

seeds did not germinate. Spat-out seeds had a higher germination percent (63.5 %) in

comparison to fecal seeds (47.2 %), but it was not statistically significant (χ2 = 2.11, df=

1, p = 0.15). However a significantly higher percentage of spat-out seeds established

(52.2 %) in comparison to fecal seeds (30.7 %) (χ2 = 5.07, df = 1, p < 0.05). Overall, 22 %

of the total number of seeds being monitored established seedlings.

2.4 Discussion

SDE criteria propose that an effective seed disperser should (i) disperse many seeds

of many species, (ii) employ handling mechanisms that do not damage seeds or have

a significant negative impact on seed germination and (iii) deposit seeds in areas

conducive for seed survival, germination and subsequent establishment (Schupp et

al., 2010). In the present study, rhesus macaques spat out or defecated (and hence

could potentially disperse) a large number of seeds of 84 % of the species they fed on

(N = 49 species), ranging in size from < 0.01 mm to 38.9 mm. Although the macaques

used defecation and spitting as dispersal mechanisms, more species (53 %) were spat

out than defecated. I did not consider dropping as a seed dispersal mechanism, as the

macaques only nibbled on the epicarp of the fruits of Dillenia indica and Castanopsis

tribuloides before discarding them and did not handle the seeds. Nearly 96 % of the

seeds handled (spat out/fecal) by rhesus macaques were undamaged. About 61 % of

32

dispersed species either had enhanced germination percentages or decreased latency

periods and rhesus seed handling was critical for three species. For the remaining 7

species, the effect of rhesus seed handling on seed germination and latency period was

neutral. Hence the results of my study establish that the rhesus macaque fulfils two of

three criteria to be assessed an effective disperser.

Long-distance dispersal has been documented to be critical to plant dynamics,

being a principal driver of population spread, persistence of subpopulation,

recolonization and gene flow (Schupp et al., 2010). Primate seed dispersal studies

employ various techniques to measure dispersal distance. Stevenson (2000), for

example, considers dispersal distance as the distance between the exact parent tree

and the point where the seed is deposited, on the condition that the focal animal fed

at one tree of a particular species only once during the sampling time and seeds of that

species were defecated/spat out for the first time in that sample 5 or more hours after

the beginning of the observations. Dispersal distances have also been calculated based

on the daily range of animals and their gut passage rates (Chapman & Russo, 2007).

Owing to the large size of our study group, and lack of information regarding rhesus

macaque gut passage rates, I did not use either of these methods in our study. Due to

similar methodological constraints, some studies (eg. Albert et al., 2013) do not report

dispersal distances of fecal seeds at all.

In general, dispersal distance of > 100 m from the parent tree is defined as long-

distance dispersal (Cain et al., 2000). However, shorter dispersal distances may also

permit seeds to escape distance and density dependent effects under parent crowns.

Appropriate dispersal distances are often species and habitat-specific (Lambert &

Chapman, 2005) and have been reported to vary between 2 and < 20 m from the crown

of the parent tree (Webb & Willson, 1985; Schupp, 1988; Ahumada et al., 2004; Hubbell

et al., 2001; Uriarte et al., 2005). In fact, it has been observed that the chance of survival

of seeds dispersed to even 5 m away from the crown is higher than that of those which

are deposited beneath it (Chapman, 1995). In this study, over 90% of all seeds (spat

out and fecal) were deposited beyond the canopy radii of feeding trees and the

maximum distance attained by dispersed seeds was 69 m for spat out seeds and 774

m for fecal seeds. Also, the assumption that the nearest adult is the parent tree

underestimates dispersal distances as the actual parent trees maybe much further

away (Nathan & Muller-Landau, 2000). Hence dispersal distances reported in this

chapter may actually be greater than what my calculations indicate.

Many studies highlight the importance of long dispersal distances away from

parental trees and negative density dependent effects (Wills et al., 1997; Cain et al.,

33

2000; Wright, 2002; Swamy & Terborgh, 2010) and macaques have been dismissed as

effective seed dispersers because they spit out a large number of seeds which are

usually not carried far from the parent tree (Balasubramanian & Bole, 1993). However

long dispersal distances of spat out seeds have been reported for macaques (265 m

by Macaca leonina- Albert et al., 2013; upto 1 km by M. fuscata- Yumoto et al., 1998) and

spitting out might confer certain benefits to seeds. Spat out seeds, for example, are

completely cleaned of their flesh and may therefore be less susceptible to fungal

attack as compared to seeds with pulp attached to them (Lambert, 2001). For the same

reason, spat out seeds would also be less attractive to seed predators, whereas

defecated seeds may attract seed predators due to the presence of dung (Andresen,

2002). Data on Prunus javanica showed that seeds dispersed by spitting by M. leonina

were deposited closer to the parent tree than seeds dispersed by hornbills and

gibbons, but accounted for 67 % of the established seedlings at the end of the year

(McConkey & Brockelman, 2011). All the monitored seeds which disappeared in the

present study were fecal seeds. Of course, these may have been removed by

secondary dispersers (Andresen, 2002) and the post-deposition seed fate of rhesus

macaque-dispersed seeds clearly requires further study.

In this study, nearly 50 % of the monitored seeds of those deposited in situ

germinated and 22 % established seedlings, thereby implying that rhesus macaques

may potentially be responsible for the emergence of a considerable number of

seedlings in tropical forests. SDE though is measured as the number of adult trees

produced by the activities of a disperser (Schupp et al., 2010) and post-deposition

seed fate estimation should essentially take into account seed survival, germination,

survival and growth of seedling to adult stage (Schupp & Fuentes, 1995). Thus, it is

imperative to carry out long-term studies to monitor establishment of adult trees

from seeds dispersed by rhesus macaques before a valid conclusion can be drawn

regarding the effectiveness of rhesus macaques as seed dispersers.

An effective frugivore should disperse the seeds of many plant species

(Andresen, 2002) but what number of species would qualify as ‘many’ would depend

on the plant community composition and fruit availability. The composition of seeds

dispersed by macaques may not be rigid but rather a function of vegetation

associated with different habitats (Tsuji et al., 2013), and further research is required

to investigate how dietary diversity and hence seed dispersal activities of rhesus

macaques may vary with resource availability (or phenological diversity) across

seasons and in different habitats. Also, mutualistic interactions like seed dispersal

involve plant species interacting with multiple frugivores, thereby forming networks

34

(Donatti et al., 2011) and certain plant-frugivore interactions maybe more specialized

and stronger than others within an assemblage (Schleuning et al., 2011). Therefore, a

complete understanding of the importance of the rhesus macaque as a seed disperser

would entail investigating the various dispersal interactions that it is a part of and

also if it links many modules within such networks. Such studies would also help

determine how vulnerable different plant species are to changes in rhesus macaque

abundance (sensu Schupp et al., 2010).

Ecologically-resilient and disturbance-tolerant primates are typically perceived

to be commonly present and therefore tend to categorised as Least Concern on the

IUCN RedList, which effectively excludes them from any conservation plans.

However, although such primate species are highly adaptable, they are also

negatively impacted by habitat degradation, poaching and indiscriminate use in

biomedical research and commercial trade (Malik, 1992; Molur et al., 2003; Eudey,

2008; Radhakrishna & Sinha, 2011; Albert et al., 2014). At least two Least Concern

species, the bonnet macaque Macaca radiata and the long-tailed macaque M.

fascicularis, have suffered major declines in population size over the past couple of

decades (Singh & Rao, 2004; Eudey, 2008; Kumara et al., 2010; Kumar et al., 2011; Singh

et al., 2011; Sengupta & Radhakrishna, 2013). A widespread geographic distribution,

and perceptions regarding its large population numbers, makes the rhesus macaque

particularly vulnerable to commodification and even a brief history of rhesus

macaque-human interactions underline an unregulated use of the species by humans

(Malik, 1992; Ahuja, 2013). More information about the ecological role of the species,

leading to a greater appreciation of its functional significance, may improve the

conservation value of the species. The results of this Chapter imply that rhesus

macaques potentially fulfil crucial ecological roles as seed dispersers, particularly in

disturbed forest areas, and I strongly urge that this parameter be considered to re-

evaluate their conservation importance in the ecosystem.

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