Ethology 90,206-224 (1992)

@ 1992 Paul Parey Scientific Publishers, Berlin and HamburgISSN 0179-1613

Biology Department, Valdosta State College, Valdosta

Ontogeny of Time Allocation in Black-tailed Prairie Dogs

W. J. LOUGHRY

LOUGHRY,W. J. 1992: Ontogeny ,of time allocation in black-tailed prairie dogs. Ethology 90,

206-224.

Abstract

The ontogeny of time allocation was studied in a field population of black-tailed prairie dogs,Cynomys ludovicianus. Pups first emerged from their natal burrows in late May. All individuals in thepopulation, including all pups, were observed for 12 weeks following this emergence. Both cross-sectional and longitudinal analyses of ontogeny revealed considerable age differences. Upon firstemergence, pups were extremely wary and spent most of their time vigilant and little time feeding. Aspups aged, they increased time spent feeding and decreased time spent vigilant. Male and female pupsbehaved similarly. Pups differed from adults in their time allocation patterns and these differenceschanged as pups aged. Pups were initially more vigilant and fed less than adults, but became lessvigilant than adults as the summer progressed. Yearlings behaved similarly to adults. Possible intrinsic(e.g., pup age and weight) and extrinsic (e.g., weather conditions, microhabitat location and coteriecomposition) influences on time allocation by pups were also examined. In general, extrinsicinfluences appeared to have more impact on pup behavior than intrinsic ones, suggesting that timeallocation by pups may be largely context-dependent. Overall, the considerable number of agedifferences argues for more consideration of ontogeny in models of antipredator behavior.

W. J. LOUGHRY, Biology Department, Valdosta State College, Valdosta, GA 31698, U.S.A.

Introduction

Of TINBERGEN'S(1963) famous four questions, ontogeny has received theleast attention from behavioral ecologists. Few studies exist of behavioraldevelopment under natural conditions, nor has ontogeny been incorporated intotheoretical models to any extent. For example, an important potential source ofselection for vulnerable young animals is predation (e.g., CHENEY& WRANGHAM1987; SULLIVAN1990). However, models of antipredator behavior, specificallythose concerning time allocation, have largely ignored ontogeny. Current modelsattempt to describe how adult individuals should apportion their time to vigilance(e.g., CARACO 1979; LIMA & DILL 1990; but see ELGAR 1989), but none provideany predictions on whether and to what extent young animals might be expected

U,S, Copyright Clearance Center Code Statement: 0179-1613/92/9003-0206$02.50/0

Prairie Dog Ontogeny 207

to differ from adults in time spent vigilant. One could argue that such considera-tions are unimportant if young animals do not differ from adults in theirbehavior. However, this argument can only be evaluated empirically. Such ananalysis can shed light on important constraints young animals face and identifythose stages in ontogeny where selection might act most strongly (e.g. SULLIVAN1988, 1990). Studies of ontogeny traditionally have employed twomethodologies: (1) description of changes in the same individuals over time, and(2) comparisons between individuals of different ages. The present study usesboth approaches in an analysis of time allocation in black-tailed prairie dogs(Cynomys ludovicianus).

Black-tailed prairie dogs are large, diurnal, non-hibernating colonialrodents. The social unit of a colony is the coterie (KING1955), which is normallycomprised of a single adult male, several adult females, and their offspring(HOOGLAND1981a). Females usually remain in the same coterie for life whereasmales typically disperse from their natal coterie as yearlings; thus coteries containmatrilines of related females (HOOGLAND1982). Pups are born in late March orearly April and first emerge from their natal burrows in mid to late May (KING1955; HOOGLAND1981a). This study describes the ontogeny of time budgets forpups during their first 12 weeks above ground and compares pup time allocationwith that of adults and yearlings over the same time period. The time budgets ofyearlings and adults are compared prior to pup emergence to determine ifdifferences between pups and adults during the pups' first summer of life lingerinto the following spring. Because time allocation by pups does change over time,important intrinsic (e.g., pup age or weight) and extrinsic (e.g., microhabitatlocation, ambient weather conditions, etc.) factors associated with this variationare also examined.

Methods

The colony of prairie dogs observed was located in Wind Cave National Park, South Dakota,and is the same colony studied by HOOGLANDsince 1974 (e.g. HOOGLAND1981a, 1986). The historyof every animal in the colony is well known and the behavior of the animals during the breedingseason and through the first emergence of pups from their natal burrows is well documented (e.g.HOOGLAND1982, 1985, 1986).

The general methods of the present study follow those of HOOGLAND(e.g., 1981a). All animalswere live-trapped, ear-tagged for permanent identification and dye-marked for long-range identifica-tion. Pups were captured within days of their first emergence above ground and prior to mixing of anylitters (n = 105 pups from 34 litters). They were also recaptured approximately every 2 wks thereafter,primarily to freshen their dye marks, but they were reweighed at these times as well.

Observations of animals commenced 4 April and ended 20 August 1989. All observationsconsisted of 5-min focal animal samples (ALTMANN1974). Data were recorded using a laptopcomputer in which each key designated a particular behavior. The activities monitored during asampling session are listed and defined in Table 1. Note that several variables were calculated bycombining the values from two or more other variables (e.g., Total Alert, Total Feed, etc.).

Samples were obtained in two slightly different ways. (1) Prior to the first emergence of pupsfrom their natal burrows, samples on adults and yearlings were obtained between 10.00 and 15.00 heach day. Each individual in the colony (n = 113 total, however, some individuals died or disappearedso that numbers for individual samples are generally slightly smaller) was observed once over a periodof 7-10 d. This sampling regime was replicated three times prior to the first emergence of pups from

208

Table 1:

W. J. LOUGHRY

Measured components of black-tailed prairie dog time budgets

DescriptionVariable

1. % Bipedal

2. % Bipedal Feed

3. % Quadrupedal

4. % QuadrupedalFeed

5. % Feed

6. % Not Vigilant

7. % Burrow

8. % Social

9. Jump-Yipping

10. Burrow Distance

11. Total Alert

12. Total Feed

13. Total Bipedal14. Total

Quadrupedal

15. Total Vigilant

percentage of time within a sample spent with only the back legs on theground and head in an alert posture (i.e., not feeding, with the plane ofthe eyes at least parallel with the ground)

same as % Bipedal except animal feeds while scanning the environment

same as % Bipedal except animal keeps all four legs in contact with theground

same as % Quadrupedal except animal feeds while scanning the envi-ronment

percentage of time within a sample time spent feeding while notscanning the environment (i.e., not vigilant)

percentage of time within a sample spent in non-feeding activities thatprecluded scanning the environment (e.g., grooming, burrow mainte-nance, etc.)

percentage of time within a sample spent within a burrow

percentage of time within a sample spent in amicable play and agonisticsocial interactions

..

animal moves from a quadrupedal stance to an extended bipedal one andcalls at the height of this jump (for complete description see SMITHet al. 1976); measured as calls per s

distance in m to the nearest burrow at the beginning of a sample

% Bipedal + % Quadrupedal

% Feed + % Bipedal Feed + % Quadrupedal Feed

% Bipedal + % Bipedal Feed

% Quadrupedal + % Quadrupedal Feed

Total Bipedal + Total Quadrupedal

their natal burrows. A fourth was finished just as pup emergence began. During the period of pupemergence, only pups were sampled until each pup had been sampled once. This took about 14 d. Forthe analysis, the fourth adult/yearling sample was combined with this pups-only sample since data forboth groups were collected during the 2-3 wk period of pup emergence. (This combined sample isreferred to as Sample 4 hereafter.) (2) Most data were collected after the final litter of pups hademerged and been captured. The colony at this time consisted of 210 animals. I divided the colony intosix groups of 35 animals each and randomly assigned each group to a particular day of observation.Individuals were not randomly assigned to groups. Rather, groups were created by adding membersfrom a coterie until the group contained 35 individuals (assignment of coteries to particular groups wasrandom). Since no coterie had 35 members, all groups were composed of individuals from more thanone coterie, and individuals in some coteries were put into different groups. All animals in the colonywere sampled over a 6-d period: two groups between 6.00-11.00 h, two between 11.00-16.00 h,and two between 16.00-21.00 h. These time blocks completely covered the daily above-groundactivity period. This schedule was rotated weekly so that over a 3-wk period each group was observedonce in each time block. This schedule of observations lasted 10 wks (from 14 June through 20August). When inclement weather precluded observing a group, the observations were made up onthe intervening day before the start of the next week's round of observations.

Each group of prairie dogs was about equally comprised of pups and adults and males andfemales. When observing any group, the order of individual observations was randomized to avoidbiasing subsets of the sampling period toward particular classes of individuals. However, an

...

Prairie Dog Ontogeny 209

observation was initiated only when an individual was visible above ground or had been observedentering a burrow just prior to the beginning of a sample. At the beginning of a sample, theindividual's location within the colony was noted, as was its distance to the nearest burrow. Inaddition, the number of other coterie members above ground at the beginning of a sample wasrecorded. For pups, this included the numbers of littermates, non-littermates, and adults present. Ialso noted whether the pup's mother was above ground at the start of the sample. Finally, the heightof the vegetation the pup was in (tall = vegetation that was taller than the top of the pup's head whilein a quadrupedal position, short = all vegetation below this point) was noted. No attempt was madeto keep track of these variables as they changed during the observation period. Information onambient weather conditions (daily minimum and maximum temperatures, relative humidity and windspeed) was obtained from the park's weather station.

Statistical analyses were carried out using the Statview statistical package. ANOV As ofdifferences between classes of prairie dogs were conducted in two ways: (1) Data from each animalover the entire study were pooled for general comparisons between age groups (pups, yearlings, andadults) and for comparisons of male versus female pups. For age comparisons, data from adults andyearlings were only pooled across those samples where pups were present above ground (i.e., Samples4-14). (2) Data from each sample were also analyzed separately, again comparing age groups (adultsversus yearlings for Samples 1-3, and versus pups for Samples 4-14) and male versus female pups(Samples 4-14). Note that for both types of analyses no individual contributed more than once to agiven data set.

Ontogenetic changes were analyzed using a repeated measures ANOV A on data collectedduring the first week pups were above ground (Sample 4) and the last week of the study (Sample 14).To further evaluate changes in pup behavior over time, Spearman rank order correlations wereperformed between sample number and pup means for each measured variable (i.e., using the data inFig. 1). A multiple regression, with intrinsic (pup age and weight) and extrinsic variables (weatherconditions and coterie composition) included, was used to identify important influences on pup timeallocation. The effects of time of day were examined by repeated-measures ANOV A using pooleddata from each individual pup at each time of day. Other extrinsic influences (presence of mother andvegetation height) were analyzed for each sample separately using t-test comparisons.

Results

"

Age Differences

Analysis of the pooled data revealed many differences between pups andadults and pups and yearlings, but none between adults and yearlings (Table 2).Adults and yearlings were more vigilant (in both bipedal and quadrupedal forms),and spent less time in burrows than did pups. In addition, adults jump-yippedmore frequently, were found farther from the nearest burrow, and spent moretime in non-vigilant activities than did pups (Table 2).

How consistent were the differences between age classes just described?Fig. 1 shows the age differences found in each sample of the study. None of themeasured variables showed a consistent age difference over the entire course ofthe study (Fig. 1). This was due in part to changes in pup behavior as they aged(see below). During their first weeks above ground, pups were more vigilant andfed less than adults. This changed rapidly so that in Sample 7 (3 weeks later) pupswere spending less time vigilant and as much time feeding as adults. Pup jump-yiprates declined from adult-like levels upon emergence to significantly lower levelsby Sample 7 (Fig. 1). As with the pooled data, few differences were foundbetween adults and yearlings, and none of the differences were consistent fromsample to sample (Fig. 1).

Ethology, Vol. 90 (3) 15

Fig. 1: X (:t SE)of all measured variables over time for each age group of prairie dogs, Data for maleand female pups are plotted separately. Statistically significant age and/or sex differences for eachsample: a = pup versus adult, b = pup versus yearling, c = yearling versus adult, and d = pup malesversuspup females.For additional information, seeTable 2. 0 adults, D yearlings, ... pup males,.

210 W. J. LOUGHRY

% BIPEDAL15

12 I aa>->- 9zUJu 6a::UJCo

3

0

% BIPEDAL FEED ..20

16

;::>- 12zUJu 8a::UJCo

4

0

TOTAL BIPEDAL

30 I b25

UJ

20

!Z 15UJ

10UJCo

5

0

TOTAL ALERT25

20>-

!z 15UJ

10UJCo

5

a

TOTAL VIGILANT

40 I '!UJ:E;:: 30>-z

20a::UJCo

1:,

..

0 i 2 3 <I is 6 7 8 9 1'0 1'1 1'2 1'3 1'4

SAMPLE

Prairie Dog Ontogeny 211

20 % QUADRUPEDALf a~b

~ 16>=I- 12zUJ

~ 8UJ

a. 4

~ 12>=

~ 20>=I- 15zUJ

~ 10UJa.

5

UJ 80::;;

>= 60I-Z

~ 40a:~ 20

0

% QUADRUPEDAL FEEDING15 d

b

TOTAL QUADRUPEDAL25

0

d

% FEED

1001

~ 80>=I- 60zUJ

~ 40UJa.

20

01

TOTAL FEED100

00 2 3 4 5 86 7 9 10 11 12 13 14

SAMPLEpup females. In sequence, sample sizes are adults: 90, 89, 88, 90, 87, 85, 83, 80, 83, 81, 82, 80, 79, 79;

yearlings: 21, 21, 21, 21,19,19,18,15,16,16,16,16,16,16; male pups: 41, 43, 48, 48, 47, 46, 46, 45,

43,43,43; female pups: 47, 48, 52, 49, 47, 46, 47, 47, 47, 47, 47. Samples 1-3 occurred before pupsfirst emerged above ground

15"-

I- 9zUJ

6()a:UJa.

3

0

212

~ 16;::,... 12z

~ 8a:wa. 4

w:; 12;::

!z 9w~ 6wa.

W. J. LOUGHRY

% NOT VIGILANT20

a

0

bd

% SOCIAL15 b,c

3

0

JUMP-YIPPING

0 0.4z0~ 0.3C/)

:;j0.2a.C/)::: 0.1<t()

0.0

BURROW DISTANCE4

..

3c

C/)a:wt;; 2:;

00 "8 9 1'0 1'1 12 131412 3 4 5 6

SAMPLE

% BURROW50

40;::,... 30zw

20wa.

10

0

Prairie Dog Ontogeny 213

Table 2: Time allocation means (S£) for each age group of prairie dogs

Significant pair-wise differences: a = pup versus adult; b = pup versus yearling (post-hoc Scheffe tests

from ANOV A using pooled data from each individual, p < 0.05); there were no significantdifferences between yearlings and adults for any of the measured variables. Sample sizes for each agegroup are given parenthetically at the top of each column. See Fig. 1 for comparisons within eachsampling period.

Sex Differences

U sing pooled data, time budgets for male and female pups did not differ forany of the measured variables (all p > 0.05). Sporadic differences emerged whensamples were examined separately, but none were consistent from sample tosample (Fig. 1). Because no consistent sex differences were found, data frommales and females were pooled in all subsequent analyses.

Ontogeny

Table 3 summarizes changes in time allocation between Sample 4 (duringpup emergence) and the end of the study (Sample 14). Pups remained close toburrows, were very vigilant and fed little upon first emerging from natal burrows.As they aged, pups moved away from burrows, fed more, and decreased the timespent vigilant and in social interactions (including jump-yipping, Table 3). Adultsshowed a similar, but less steep, decline in these variables as the summerprogressed (Fig. 1). Thus, pups started the summer being more vigilant andfeeding less than adults and ended feeding more and being less vigilant thanadults.

To evaluate whether pup behavior changed consistently over time, I per-formed Spearman rank correlations of pooled pup means for each variable, usingsample number as the independent variable. Only four statistically significantrelationships were obtained (Table 3): time spent feeding (% feed and total feed)and distance from the nearest burrow increased and the rate of jump-yippingdecreased as pups aged.

Variable Pups (103) Yearlings (21) Adults (90) Differences

% Bipedal 2.86 (0.18) 5.26 (1.04) 6.02 (0.57) a, b% Bipedal Feed 8.90 (0.30) 8.25 (0.82) 6.81 (0.41) a

% Quadrupedal 3.53 (0.41) 3.58 (0.77) 3.36 (0.37) none

% Quadrupedal Feed 3.69 (0.16) 6.42 (0.47) 5.69 (0.27) a, b% Feed 58.21 (1.01) 57.53 (2.31) 57.20 (1.33) none

% Not Vigilant 4.53 (0.61) 6.51 (1.01) 6.02 (0.44) none% Burrow 14.71 (0.68) 7.72 (1.32) 11.41 (0.90) a, b% Social 2.72 (0.25) 3.93 (1.45) 2.52 (0.45) none

Jump-Yipping 0.09 (0.01) 0.13 (0.02) 0.15 (0.01) aBurrow Distance 1.97 (0.05) 2.26 (0.12) 2.36 (0.06) aTotal Alert 6.40 (0.46) 8.83 (1.40) 9.38 (0.75) aTotal Feed 70.80 (1.08) 72.20 (2.54) 69.70 (1.46) none

Total Bipedal 11.78 (0.38) 13.51 (1.31) 12.83 (0.76) none

Total Quadrupedal 7.22 (0.42) 9.98 (0.97) 9.04 (0.42) a, b

Total Vigilant 19.00 (0.55) 23.50 (1.63) 21.87 (0.85) a, b

Ontogenetic differences: paired t-test, n = 77; Sample 4: the beginning of pup emergence from natalburrows; Sample 14: the end of the study 12 wks later. The direction of significant (p < 0.05)differences is indicated. Spearman rank correlations compare means of each measured variable (fromFig. 1) with time (i.e., samples, see Fig. 1). The effects of mother's presence and vegetation height arebased on t-test comparisons done for each sample separately. The direction of each significantdifference (p < 0.05) and the sample number in which the difference was obtained are shown. P:mother present; NP: mother not present; T: tall vegetation; S: short vegetation; " p < 0.05.

ExtrinsicInfluenceson Time Allocation

Does the presence of a pup's mother above ground affect how the pupbehaves? Comparisons of pup time allocation when the mother was above groundversus when the mother was absent indicate the answer is no (Table 3). Fewdifferences were found and they were rarely consistent fom sample to sample(Table 3). However, the general pattern when differences did occur was for pupsto feed more, be less vigilant and move further from burrows when the motherwas present (Table 3; sample sizes for when the mother was present ranged from57-74, and 17-35 when she was absent).

Vegetation height (tall versus short) also affected pup behavior (Table 3).Generally speaking, pups increased the time spent in bipedal forms of vigilance(% bipedal feed, total bipedal) and increased their total allocation of time tovigilance (Table 3) when in tall vegetation. Pups also fed more, were further fromand spent less time in burrows, and spent less time in non-vigilant activities whilein tall grass (Table 3). However, these general patterns were not present in allsamples and in some samples the pattern was reversed (e.g., % feed). This couldbe due to small numbers of pups in tall vegetation in later sampling periods (meannumber of pups observed in tall vegetation in Samples 4-8 = 34.2, in Samples

..

214 w. J. LOUGHRY

Table3: Temporal changes in pup time budgets and the effects of mother's presence and vegetationheight on pup time allocation

Ontogenetic Mother's VegetationVariable differences r, presence height

% Bipedal ns 0.07 NP > P (14) T> S (13), S > T (5, 14)% Bipedal Feed ns -0.27 NP > P (12) T> S (6, 7, 8,9, 11, 13, 14)% Quadrupedal 4> 14 -0.49 none none

% Quadrupedal Feed 14> 4 0.31 NP > P (12) S > T (5)% Feed 14> 4 0.68"- P > NP (8, 14) T> S (4, 5, 7), S > T (9, 14)% Not Vigilant 4> 14 0.05 none S > T (7)% Burrow ns -0.40 NP > P (8, 14) S > T (5, 7, 8)% Social 4> 14 -0.35 NP> P (4) none

jump-Yipping 4> 14 -0.67" NP > P (12) noneBurrow Distance 14> 4 0.59" P > NP (7, 14), T> S (4, 5, 6)

NP > P (10)Total Alert 4> 14 -0.33 none S > T (14)Total Feed 14 > 4 0.80" P > NP (8, 14) T> S (4, 5, 7, 8)Total Bipedal ns -0.09 NP > P (12) T > S (6, 7, 8, 9, 11, 13, 14)Total Quadrupedal 4> 14 -0.25 none S > T (6)Total Vigilant 4> 14 -0.13 NP > P (12) T > S (7, 8, 13, 14)

Prairie Dog Ontogeny 215

9-14 = 11.0; sample sizes for pups in short vegetation ranged from 45-87, andfrom 6-46 in tall vegetation). While a lack of pups in tall vegetation presents aproblem for statistical analyses, it may not reflect a shift in microhabitat usage bypups, since what was once tall vegetation for pups may become short due to theincrease in pup body size.

Time of day was another important influence on pup time allocation. Atleast some pups were active as much as 30 min before sunrise and for up to 30 minafter sunset each day (LOUGHRY,unpubl. data). Early in the day, pups were morevigilant, especially while feeding, than they were during the middle of the day orin the evening (Table 4). Mid-day seemed to be a time of decreased activity, withpups remaining close to burrows and spending more time underground (Table 4).By late afternoon and evening, pups resumed above-ground activity, but concen-trated on feeding and spent little time vigilant (Table 4).

MultipleRegression Analyses

Other extrinsic factors (e.g., ambient weather conditions) as well as intrinsicones (e.g., pup age or weight) could also influence pup time allocation. As ameans of assessing their potential importance, I ran a multiple regression of eachmeasured variable against these other factors. The analyses revealed a statisticallysignificant multiple r value for every variable (Table 5). However, these regres-sions may be significant primarily because of large sample sizes, since the amountof variation explained for each variable is small (Table 5). Keeping this in mind, ifone first looks at intrinsic influences, pup age (in days since first emergence fromnatal burrow, range: 1-87 d) was positively associated with time spent feeding,

Table 4: Means (SE) of pup time allocation at different times of day

Significant pair-wise differences: a = morning versus mid-day, b = morning versus evening, and c =mid-day versus evening (post-hoc Scheffe tests from repeated measures ANOV A using pooled datafrom each individual at each time of day, n = 98, P < 0.05).

Variable Morning Mid-day Evening Differences

% Bipedal 3.44 (0.37) 3.36 (0.29) 1.72 (0.25) b, c% Bipedal Feed 10.58 (0.52) 8.68 (0.47) 6.92 (0.41) a, b, c% Quadrupedal 3.34 (0.57) 4.32 (0.54) 1.36 (0.33) b, c% Quadrupedal Feed 5.17 (0.27) 2.72 (0.20) 3.42 (0.22) a, b, c% Feed 67.11 (1.27) 45.58 (1.67) 68.94 (1.56) a, c% Not Vigilant 4.18 (0.44) 4.66 (0.37) 2.45 (0.27) b, c% Burrow 2.21 (0.60) 26.26 (1.53) 12.85 (1.44) a, b, c% Social 2.93 (0.49) 3.75 (0.50) 1.52 (0.39) c

Jump- Yipping 0.06 (0.01) 0.09 (0.01) 0.09 (0.01) noneBurrow Distance 2.08 (0.07) 1.74 (0.06) 2.19 (0.07) a, cTotal Alert 6.77 (0.76) 7.68 (0.57) 3.13 (0.46) b, cTotal Feed 82.86 (1.32) 56.98 (1.95) 79.28 (1.61) a, c

Total Bipedal 14.01 (0.68) 12.04 (0.60) 8.69 (0.48) a, b, cTotal Quadrupedal 8.52 (0.61) 7.05 (0.54) 4.78 (0.39) b, cTotal Vigilant 22.53 (0.93) 19.09 (0.65) 13.47 (0.64) a, b, c

216 w. J. LOUGHRY

and negatively with time spent in burrows and the rate of jump-yipping (Table 4).Pup weight (range: 90-450 g) was positively related to time spent in quadrupedalvigilance (Table 5).

While intrinsic factors did have some influence on time allocation, extrinsicones seemed much more important (Table 5). However, even among theseextrinsic factors, some appeared more important than others. For example, thenumber of adult coterie members present above ground (range: 0-11) correlatedmore strongly with aspects of pup time allocation than did either the number oflittermates (sibs, range: 0-6) or non-littermates present (non-sibs, range: 0-22;see Table 5). With more adults present, pups were found further from burrows,were less vigilant and fed more. Even more important than coterie compositionwere ambient weather conditions: pups were more vigilant on windy days (range:1.6-29 km per h), fed more on cool days (range of minimum temperatures:0-21 DC), and spent more time in burrows on hot days (range of maximumtemperatures: 20-43 °C). Only relative humidity (ranging from 12-100 %) hadlittle impact on pup time budgets (Table 5).

A final influence on pup time allocation was the distance a pup was from thenearest burrow (Table 5). When pups were further from burrows they fed more,were less vigilant and jump-yipped less frequently. Judging from the partial F-ratios obtained in this analysis, distance from the nearest burrow was one of themost important influences on pup time allocation (Table 5).

Discussion

The present study leads to the following conclusions: (1) differences betweenpup and adult black-tailed prairie dogs in time allocation occur throughout muchof the pups' first summer above ground; (2) the particular age differences foundand the direction of these differences change as a result of temporal changes inboth pup and adult behavior; (3) by the following spring, time budgets of pups(now yearlings) do not differ much from those of adults, so pups must begin toreach adult-like levels of time allocation during the fall or winter (indeed, pupsalready appear to behave much like adults within a month or so of firstemergence, see Fig. 1); (4) the presence of the mother above ground has littleimpact on pup time allocation; (5) vegetation height affects pup behavior, but aspups age they are rarely found in tall vegetation; (6) pups behave differently atdifferent times of day; and (7) while pup age and weight are both correlated withsome aspects of time allocation, extrinsic influences such as microhabitat location,ambient weather conditions, and number of adults present seem much moreImportant.

Antipredator behavior in prairie dogs has received considerable attention(HOOGLAND1979, 1981b; DEVENPORT1986, 1989). For example, HOOGLAND(1979) documented several influences on prairie dog vigilance: individuals spentless time vigilant in colonies of larger size, when at the center of a colony versusthe edge, and after the emergence of pups (young of the year) from their natal

...

Table 5: Partial F-ratios from multiple regression analyses (df = 10, 1015) of potential influences on pup time allocation for each measured variable

':-p < 0.05; ,',' P < 0.01.

>-.:J.....i:j';;.

v0

(JQ0::>8

(JQ'"::>

'<

N......'-J

Pup Pup Burrow Wind Min. Max. % No. No. No.Variable Multiple r age weight distance speed temp. temp. humidity adults sibs non-sibs

% Bipedal 0.18*" 1.84 0.08 18.17"" 2.27 0.95 0.90 0.003 6.54"" 0.17 1.43

% Bipedal Feed 0.17':":' 1.47 0.97 1.76 4.92" 10.98':'" 0.34 0.13 0.02 0.07 3.82"

% Quadrupedal 0.38'-':- 2.55 5.65" 20.15*" 10.47':-* 1.18 5.01" 1.41 2.97 1.08 0.74

% Quadrupedal Feed 0.19':-" 11.09"':- 0.18 0.40 0.68 0.09 3.31 5.32" 0.88 0.002 4.55':-% Feed 0.38':-" 10.14"" 0.02 47.95"" 3.26 19.44"" 9.28'-"- 0.002 18.36"':- 4.23':- 0.70

% Not Vigilant 0.20':-" 0.47 0.24 14.34"" 0.12 0.01 0.05 3.80" 4.90" 0.14 12.81"':-% Burrow 0.32"':- 12.95':-" 0.41 11.93"" 16.96':-" 3.69 16.50':-" 1.27 8.29':":- 3.12 0.01% Social 0.16"':- 1.45 0.03 1.93 0.13 1.44 2.35 0.76 0.31 0.001 3.26

Jump-Yipping 0.22"':- 15.79"" 0.09 4.38" 0.42 0.80 1.38 1.74 0.15 0.54 0.003Burrow Distance 0.24"'- 2.15 3.67 0.19 0.39 2.71 1.71 23.98"" 5.11" 0.89Total Alert 0.35"':- 0.29 3.01 34.16"" 11.38"" 1.91 1.60 0.94 7.50'H' 1.09 1.75

Total Bipedal 0.17"-" 3.29 0.99 1.88 7.56"" 11.29'-" 1.09 0.11 2.59 0.003 0.90

Total Quadrupedal 0.37':-':- 0.003 5.74" 19.86"" 11.36':-" 0.78 8.23"':- 4.40" 1.45 0.90 0.01

Total Vigilant 0.34':-" 1.78 0.86 17.33"" 19.76"" 10.00"':- 1.49 2.97 4.25" 0.46 0.64Total Feed 0.35'-':- 12.79"" 0.01 39.91"" 5.41" 8.47"-" 7.45':-':- 0.14 14.55':-" 3.50 2.52

218 w. J. LOUGHRY

.burrows (presumably because colony size increased). These findings were basedon data pooled across all age groups (although, apparently, pups were rarelyincluded) and differences between different classes of individuals were notexamined. It is conceivable, and indeed likely, that such differences exist and playan important role in influencing antipredator behavior. For example, the declinein individual vigilance coincident with the emergence of pups seems paradoxicalsince pups of many ground squirrels are extremely vulnerable during their firstfew weeks above ground (FITCH 1948; ROBINSON1980; OWINGS& LOUGHRY1985; LOUGHRY1987; LOUGHRY& McDONOUGH 1989; HOOGLAND,unpubl.data). In fact, as this study has shown, this decline may only be apparent amongcertain individuals. Certainly pups themselves show very high levels of vigilanceimmediately after emergence and it may be that parents are also more alert at thistime (LOUGHRY,unpubl. data). Lumping data from all individuals obscures suchpotentially interesting differences.

Age Differences

There are a number of reports of age differences in time allocation orantipredator behavior (e.g., CAREY& MOORE1986; FERGUSON1987; HEINSOHN1987; SULLIVAN1988, 1990; FRAGASZY1990). In some species, young animals areless vigilant than adults and in others they are more vigilant. As stated earlier,theory provides no clear predictions about when to expect either of these results.In the present study, black-tailed prairie dog pups showed both patterns atdifferent points in development. This argues against any easy prediction of whenand where to expect particular age differences in behavior and instead implies thatsuch differences may be context- rather than species-specific.

Sex Differences

Male and female pups differed little in their time budgets over the course ofthis study. Similar results were obtained for a different population of black-tailedprairie dogs (DEVENPORT1986), and in California ground squirrels (Spermophilusbeecheyi, LOUGHRY& McDONOUGH1989). Sex differences have been found inother ground squirrel species when looking at a particular type of behavior suchas play (e.g., NOWICKI& ARMITAGE1979; JAMIESON& ARMITAGE1987; WATER-MAN 1988). In the present study, play occurred too rarely to be analyzedseparately. Detailed analysis of a particular behavior may be necessary to uncoversex differences early in ontogeny. Alternatively, such differences may not emergeuntil later in development. Preliminary comparison of yearling male and femaleblack-tailed prairie dogs also shows few sex differences in time budgets, but adultmales differ substantially from adult females (LOUGHRY,unpubl. data). Thissuggests that sex differences in prairie dog behavior do in fact emerge late inontogeny, perhaps tied to the acquisition of reproductive status by the males.

Ontogenetic Changes

Time budgets of pups changed significantly over the course of the summer.Pups were more vigilant and fed little upon first emerging from natal burrows,

Prairie Dog Ontogeny 219

but as they aged pups increased time spent feeding and decreased time spentvigilant. High levels of vigilance early in ontogeny are not suprising if oneassumes that pups are more vulnerable to predation (OWINGS& LOUGHRY1985;LOUGHRY1987; HOOGLANDunpubl. data). This could be due to their small size,which may make them vulnerable to a wider array of predators, and/or to a lack ofknowledge about the environment. As pups age and grow larger, vulnerabilitypresumably declines and the most important consideration may become foodacquisition. This might be especially important if increased feeding leads toincreased mass and heavier pups are better able to survive the coming winter(MURIE& BOAG1984; MICHENER& LOCKLEAR1990). In this regard, note thatpup age but not pup weight was significantly correlated with time spent feeding(% quadrupedal feed, % feed, total feed) in the multiple regression analysis. Thissuggests that as pups age they increase time spent feeding regardless of how heavythey already are, and points again to the probable importance of mass accumula-tion for pups.

The initial analysis of ontogenetic changes focused on differences betweenthe first weeks pups were above ground and the last week of the study. Such ananalysis ignores the considerable week to week variation that occurred (seeFig. 1). Thus, discussion of significant ontogenetic changes over the course of thesummer may be misleading. The same pattern of differences might not haveemerged had the study concluded one week earlier or later. Indeed, the onlyconsistent changes over the entire course of the study were for feeding anddistance from the nearest burrow to increase, and the rate of jump-yipping todecrease as pups aged. These first two patterns are common among groundsquirrels (see e.g., MICHENER1981; BARASH1989). In black-tailed prairie dogs,these changes may be due to decreasing vulnerability of pups to predation and aconcomitant emphasis on energy accumulation in preparation for winter. Anexplanation for the decrease in jump-yipping is less apparent. Jump-yipping bypups appears to be a powerful elicitor of attention from adults when pups firstemerge from natal burrows (pers. obs.). At this time, when a pup calls, one ormore of the adults of the coterie, and particularly the pup's mother, willimmediately run over to the pup, apparently to investigate what precipitated thecalls. It could be that adults eventually habituate to pup jump-yips, making thecalls less effective so that pups give up on calling as a means of eliciting adultattention. However, the potential communicative functions of jump-yipping arestill unclear and any explanation of changes in this form of calling must remaintentative.

Extrinsic Influences on Time Allocation

One of the more surprising findings of this study was that time budgets ofpups appeared to correlate more with extrinsic rather than intrinsic factors (d.FRAGASZY1990). This implies that pup time allocation has less to do withindividual identity and more to do with the environmental context in which thepup finds itself. With regard to extrinsic influences, the finding that pups areinfluenced by the number of other adults, but not by the number of other litter ornon-litter mates present above ground, has an important implication. Many

220 W. J. LOUGHRY

studies have shown a negative relationship between group size and time spentvigilant (reviewed in ELGAR1989; LIMA1990; LIMA& DILL1990). However, thisimplies that all members of a group are considered equal. The present resultssuggest that overall group size may not be as important as the number of certainindividuals in the group, implying a difference between absolute group size andwhat could be called "effective" group size (d. LIMA1990). For many speciesliving in large colonies, the existence of some effective group size, comprised of aparticular subset of colony members, seems an important possibility that requiresfurther study. For example, in black-tailed prairie dogs, DEVENPORT(1989)reported a positive relationship between an individual's distance to the nearestburrow and the number of other animals above ground. The results of the presentstudy suggest that absolute numbers of other animals may not be as important asnumbers of particular classes of individuals.

While the number of adults above ground was significantly associated withtime allocation of pups, there was no evidence that a particular adult was moreimportant than any others to pups. Specifically, the presence of a pup's motherabove ground had little impact on its behavior. This may not be surprising in lightof the fact that mothers appear to interact little with their pups once they comeabove ground (LOUGHRY,unpubl. data). Also, adult female coterie members aregenetically related (HOOGLAND1982), so for pups, adult females may all beregarded as equivalent. Thus, the presence of any particular female may not be asimportant as the absolute number of adult females present. There is evidence tosuggest that if any particular adult within a coterie is more important than theothers it may be the coterie's resident adult male (LOUGHRY,unpubl. data). Adultmales spend more time vigilant than any other age or sex group (LOUGHRY,unpubl. data), and their presence above ground may allow pups to evaluate theriskiness of continuing above-ground activity. Further experiments are needed totest this hypothesis.

Ambient weather conditions also influenced time allocation. For example,pups were more vigilant on windy days. High wind speeds may create a noisyenvironment in which the approach of potential predators is harder to detectaurally. Under such conditions, individuals may increase their time spent vigilantin order to increase the chances of visual detection of predators. Temperatureaffected pup time allocation in two ways: pups fed more on days with coolerminimum temperatures and spent more time in burrows on days with highermaximum temperatures. This latter result is consistent with the finding that pupsalso spent more time in burrows during the middle of the day than in either themorning or evening. Pups can die as the result of prolonged exposure to the sunon hot days (pers. obs.), so increasing time below ground may have importantsurvival consequences. Minimum temperature typically occurred at night, andpups spent more time feeding the subsequent day. Pups avoid the potentially highcosts of thermoregulation over night by sleeping together in burrows (HOOGLAND1981a; pers. obs.). However, if cold nights are also associated with cool days,then pups may face increased energetic requirements for thermoregulation duringthe day, which may be met by increasing feeding time (see also LIMA1988;KENAGYet al. 1989).

.'

..

to.

Prairie Dog Ontogeny 221

Distance to the nearest burrow was one of the more important influences ontime allocation and has been shown to be important in other ground squirrels(LEGERet al. 1983; HOLMES1984; CAREY1985). However, these other studieshave generally found a positive relationship between distance to the nearestburrow and time spent vigilant. Contrary to these reports, the present studyuncovered a negative relationship. This is probably because pups use burrows aspromontories from which to scan the environment. Other ground squirrels donot construct burrow mounds to the same extent as black-tails and, presumablythen, cannot use them for surveying their surroundings. Because of their smallbody size, pups may only be able to scan their surroundings when on burrows,thus producing the negative relationship found here.

Pups did not completely abandon vigilant activities when off burrows. Forexample, pup vigilance was apparently influenced by the height of the vegetationthe pup was in. Specifically, pups increased bipedal forms of vigilance in tallvegetation, presumably because they could not otherwise scan the environment atall in this microhabitat. Assuming that being in tall vegetation makes pups morevulnerable to ambush by predators, it still appears necessary for pups to spendtime there in order to acquire the resources necessary for growth. Pups mayattempt to trade-off this increased risk by increasing time spent vigilant, particu-larly while feeding (note that time spent bipedally feeding is the variable appa-rently most impacted by a pup's presence in tall grass, Table 3).

Finally, time of day also affected pup time allocation. Early morning was atime of much activity and pups exhibited high levels of vigilance, feeding andother activities (see Table 5). High feeding levels are to be expected if pups haveburned most energy stores during the night and come above ground needing toreplenish them. However, ambient light conditions are still low, so high vigilancelevels might also be expected since predation risk is presumably high at this timealso (LIMA1988). During the heat of the day, activity decreased and pups spentmore time in or near burrows. Prolonged exposure to the sun on hot days can bedetrimental to pups (see above), so this seems to make sense. By evening pupsresumed above-ground activity but concentrated on feeding and little else. Thislast finding is surprising since, just as in the morning, evening is a time of lessambient light and presumed higher risk from predators. Possibly pups are feedingso much in order to accumulate energy reserves to get them through the coolnight, although this seems unnecessary given that pups spend nights together inburrows (see above).

Conclusions

Summarizing the present findings, black-tailed prairie dog pups appear tomove from a state of high vulnerability to predation, during which they behavecautiously, to a state of lessened vulnerability where the main emphasis appears tobe on feeding and accumulating enough body mass to survive the coming winter.While these are the general ontogenetic trends, the particular pattern of timeallocation that a pup exhibits on any given day appears to be largely the productof a particular environmental context, rather than something intrinsic to the pup.

222 W. J. LOUGHRY

More generally, the results of this study suggest that ontogenetic differencesneed to be incorporated into models of time allocation. Cross-sectional analyseshighlight the importance of age class differences in understanding time allocationby prairie dogs. In addition, not only do age groups vary from one another, butindividuals can change substantially over time. Variability, in the form of the age-related differences reported here or even between individuals within a particularage class, has been argued to have important consequences for our understandingof many different kinds of behavior (e.g., ARMITAGE1982; CLARK& EHLINGER1987; RITCHIE1988; BARASH1989). In the present case, it would appear necessaryto incorporate such findings into any attempts to model antipredator behavior.While a few attempts have been made (e.g., WERNER& GILLIAM1984), we stillhave limited tools for predicting if and when ontogenetic differences might occurand what their functional significance might be.

.

Acknowledgments

This work was partially supported by an N. 1. H. post-doctoral trainees hip in ethologyprovided by the University of Tennessee. I thank the staff of Wind Cave National Park, and especiallythe director, E. ORTEGA,for their support of this project. S. D. KILDAWprovided assistance duringthe early stages of the study. Most importantly, I thankJ. HOOGLANDfor the invitation to work withhis study animals and for some crucial mid-summer aid in re-marking animals. S. L. BROWNand R. A.MORGAN provided support during the early stages of manuscript preparation while I was atSouthwestern University. J. HOOGLAND,P. T. LOPEZ,C. M. MCDONOUGH,D. H. OWINGSand J.RASMUSSENthoroughly reviewed earlier versions of this paper.

Literature Cited

ALTMANN,J. 1974: Observational study of behavior: sampling methods. Behaviour 49, 227-265.ARMITAGE,K. B. 1982: Social dynamics of juvenile marmots: role of kinship and individual

variability. Behav. Ecol. Sociobiol. 11, 33-36.BARASH,D. P. 1989: Marmots: Social Behavior and Ecology. Stanford Univ. Press, Stanford.CARACO,T. 1979: Time budgeting and group size: a theory. Ecology 60, 611-617.CAREY,H. V. 1985: The use of foraging areas by yellow-bellied marmots. Oikos 44, 273-279.- - & MOORE,P. 1986: Foraging and predation risk in yellow-bellied marmots. Am. MidI. Nat.

116, 267-275.CHENEY, D. L. & WRANGHAM,R. W. 1987: Predation. In: Primate Societies. (SMUTS,B. B.,

CHENEY,D. L., SEYFARTH,R. M., WRANGHAM,R. W. & STRUSAKER,T. T., eds.) Univ. ofChicago Press, Chicago, pp. 227-239.

CLARK,A. B. & EHLINGER,T. J. 1987: Pattern and adaptation in individual behavioral differences.In: Perspectives in Ethology. Vol. 7. Alternatives. (BATESON,P. P. G. & KLOPFER,P. H.,eds.) Plenum Press, New York, pp. 1-47.

DEVENPORT,J. A. 1986: Foraging and behavioral ecology of black-tailed prairie dogs. Unpubl. Ph.D.Diss., Univ. of Oklahoma, Norman.

- - 1989: Social influences on foraging in black-tailed prairie dogs. J. Mammal. 70, 166-168.ELGAR,M. 1989: Predator vigilance and group size in mammals and birds: a critical review of the

empirical evidence. BioI. Rev. 64, 13-33.FERGUSON,J. W. H. 1987: Vigilance behaviour in white-browed sparrow-weavers Plocepasser

mahali. Ethology 76, 223-235.FITCH, H. S. 1948: Ecology of the California ground squirrel on grazing'lands. Am. MidI. Nat. 41,

513-596.

FRAGASZY,D. M. 1990: Sex and age differences in the organization of behavior in wedge-cappedcapuchins, Cebus olivaceus. Behav. Ecol. 1, 81-94.

.

...

Prairie Dog Ontogeny 223

HEINSOHN,R. G. 1987: Age-dependent vigilance in winter aggregations of cooperatively breeding. white-winged choughs (Corcorax melanorhamphos). Behav. Ecol. Sociobiol. 20, 303-306.

HOLMES,W. G. 1984: Predation risk and foraging behavior of the hoary marmot in Alaska. Behav.Eco!' Sociobiol. 15, 293-30l.

HOOGLAND,J. L. 1979: The effect of colony size on individual alertness of prairie dogs (Sciuridae:Cynomys spp.). Anim. Behav. 27, 394-407.

1981a: Nepotism and cooperative breeding in the black-tailed prairie dog (Sciuridae: Cynomysludovicianus). In: Natural Selection and Social Behavior: Recent Research and Theory.(ALEXANDER,R. D. & TINKLE,D. W., eds.) Chiron Press, New York, pp. 283-310.1981b: The evolution of coloniality in white-tailed and black-tailed prairie dogs (Sciuridae:Cynomys leucurus and Cynomys ludovicianus). Ecology 62, 252-272.1982: Prairie dogs avoid extreme inbreeding. Science 215, 1639-164l.1985: Infanticide in prairie dogs: lactating females kill offspring of close kin. Science 230,1037-1040.

1986: Nepotism in prairie dogs (Cynomys ludovicianus) varies with competition but not withkinship. Anim. Behav. 34, 263-270.

JAMIESON,S. H. & ARMITAGE,K. B. 1987: Sex differences in the play behavior of yearling yellow-bellied marmots. Ethology 74, 237-253.

KENAGY,G. J., SHARBAUGH,S. M. & NAGY, K. A. 1989: Annual cycle of energy and timeexpenditure in a golden-mantled ground squirrel population. Oecologia 78, 269-282.

KING, J. A. 1955: Social behavior, social organization, and population dynamics in a black-tailedprairie dog town in the Black Hills of South Dakota. Contr. Lab. Vert. Bio!., Univ. Michigan67, 1-123.

LEGER, D. W., OWINGS, D. H. & COSS, R. G. 1983: Behavioral ecology of time allocation inCalifornia ground squirrels (Spermophilus beecheyi): microhabitat effects. J. Compo Psycho!.97, 283-29l.

LIMA, S. L. 1988: Vigilance during the initiation of daily feeding in dark-eyed juncos. Oikos 53,12-16.

1990: The influence of models on the interpretation of vigilance. In: Interpretation andExplanation in the Study of Animal Behavior. Vo!. 2. Explanation, Evolution, and Adapta-tion. (BEKOFF,M. & JAMIESON,D., eds.) Westview Press. Boulder, pp. 246-267.& DILL, L. M. 1990: Behavioral decisions made under the risk of predation: a review andprospectus. Can. J. Zool. 68, 619-640.

LOUGHRY,W. J. 1987: The dynamics of snake harassment by black-tailed prairie dogs. Behaviour103, 27-48.

- - & McDONOUGH, C. M. 1989: Calling and vigilance in California ground squirrels: age, sexand seasonal differences in responses to calls. Am. MidI. Nat. 121, 312-32l.

MICHENER,G. R. 1981: Ontogeny of spatial relationships and social behaviour in juvenile Richard-son's ground squirrels. Can. J. Zoo!. 59, 1666-1676.

- - & LOCKLEAR,L. 1990: Differential costs of reproductive effort for male and female Richard-son's ground squirrels. Ecology 71, 855-868.

MURIE,J. O. & BOAG, D. A. 1984: The relationship of body weight to overwinter survival inColumbian ground squirrels. J. Mamma!. 65, 688-690.

NOWICKI,S. & ARMITAGE,K. B. 1979: Behavior of juvenile yellow-bellied marmots: play and socialintegration. Z. Tierpsychol. 51, 85-105.

OWINGS,D. H. & LOUGHRY,W. J. 1985: Variation in snake-elicited jump-yipping by black-tailedprairie dogs: ontogeny and snake specificity. Z. Tierpsycho!. 70, 177-200.

RITCHIE,M. E. 1988: Individual variation in the ability of Columbian ground squirrels to select anoptimal diet. Evo!' Eco!' 2, 232-252.

ROBINSON,S. R. 1980: Antipredator behaviour and predator recognition in Belding's ground squirre!.Anim. Behav. 28, 840-852.

SMITH,W. J., SMITH,S. L., DEVILLA,J. G. & OPPENHEIMER,E. C. 1976: The jump-yip display ofthe black-tailed prairie dog, Cynomys ludovicianus. Anim. Behav. 24, 609-62l.

SULLIVAN,K. A. 1988: Ontogeny of time budgets in yellow-eyed juncos: adaptation to ecologicalconstraints. Ecology 69, 118-124.1990: Daily time allocation among adult and immature yellow-eyed juncos over the breedingseason. Anim. Behav. 39, 380-387.

224 W. J. LOUGHRY, Prairie Dog Ontogeny

.TINBERGEN,N. 1963: On aims and methods of ethology. Z. Tierpsychol. 20, 410-433.WATERMAN,J. M. 1988: Social play in free-ranging Columbian ground squirrels, Spermophilus

columbianus. Ethology 77, 225-236.WERNER,E. E. & GILLIAM,J. F. 1984: The ontogenetic niche and species interactions in size-

structured populations. Ann. Rev. Ecol. Syst. 15, 393-425.

Received: July 29, 1991

Accepted: December 28, 1991 (j. Brockmann)

.

-

,.

.