factors affecting pup growth and survival in co-operatively breeding meerkats suricata suricatta

Journal of Animal Ecology

2002

71

, 700–709

© 2002 British Ecological Society

Blackwell Science, Ltd

Factors affecting pup growth and survival in co-operatively breeding meerkats

Suricata suricatta

A. F. RUSSELL, T. H. CLUTTON-BROCK, P. N. M. BROTHERTON, L. L. SHARPE*, G. M. MCILRATH†, F. D. DALERUM†, E. Z. CAMERON† and J. A. BARNARD

Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK;

*

Department of Zoology, University of Stellenbosch, Matieland 7602, Republic of South Africa; and

†

Mammal Research Institute, University of Pretoria, Pretoria 0002, Republic of South Africa

Summary

1.

We examined the relative importance of maternal, environmental and social factorsfor post-weaning pup growth and survival in a co-operatively breeding mammal, themeerkat

Suricata suricatta

.

2.

Pup daily weight gain was primarily influenced by the number of carers per pup andthe daily weight gain of those carers. Rainfall and daily temperatures had additionalpositive and negative effects, respectively, on weight gain of pups born to subordinates.

3.

Pup overnight weight loss was primarily influenced by the amount of weight pupsgained during the day, and their age. However, pups also lost considerably more weightovernight when temperatures were cold, although such effects were less in large groups.

4.

Pup growth rates were positively influenced by the number of carers per pup andcarer condition, and negatively influenced by high daytime temperatures.

5.

Pup weight at independence was positively associated with weight at emergence andpup weight gain during provisioning, but negatively associated with the extent of over-night weight loss.

6.

Pup survival between emergence and independence was related to maternal status,pup sex and overnight weight loss, as well as to group size, daytime temperature andmonthly rainfall.

7.

Thus, in meerkats, social factors largely, but not wholly, replace the importance ofmaternal factors that are commonly found to govern reproductive success in non-co-operatively breeding social vertebrates.

Key-words

: condition, helpers, kin selection, maternal, social, weight.


(2002)

71

, 700–709

Introduction

Lifetime reproductive success, one of the most com-plete measures of fitness currently available, is associ-ated with the number and condition of offspring thatan individual raises to independence (Clutton-Brock1988). Studies over the last 20 years have shown thatearly development is a significant contributor of over-all differences in lifetime reproductive success betweenindividuals and cohorts (Clutton-Brock 1991; Lind-ström 1999). Phenotypic and environmental factorsthat affect a mother’s capacity to invest in her offspringcommonly have an important influence on an off-

spring’s early development (Clutton-Brock 1991) and,through this, affect many aspects of its subsequent sur-vival and reproductive success (Lummaa & Clutton-Brock 2002). For example, in red deer

Cervus elephus

L., warm temperatures during spring enhance foodavailability in the last few months of gestation, generatingcohorts of calves with relatively heavy birth weights(Albon, Clutton-Brock & Guinness 1987). Not onlydoes increased birth weight reduce an individual’sprobability of dying in its first year of life (Guinness,Clutton-Brock & Albon 1978), but it also leads to arelatively large adult size and a subsequent productionof relatively heavy calves. (Albon

et al

. 1987).While environmental and maternal characteristics

exert a strong effect on offspring in social mammalswhere offspring are raised primarily by their parent(s),in co-operative breeders, where offspring derive much

Correspondence Andrew F. Russell, Department of Zoology,University of Cambridge, Cambridge CB2 3EJ, UK (fax +441223 336676; e-mail [email protected]).

JAE_636.fm Page 700 Tuesday, July 2, 2002 9:25 AM

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© 2002 British Ecological Society,


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of their food from helpers, early development might beexpected to be primarily influenced by the number ofhelpers available to feed the young. Indeed, many stud-ies of co-operative breeders reveal positive relation-ships between helper number and reproductive success(Emlen 1991; Jennions & Macdonald 1994). However,the importance of such social effects for reproductivesuccess, compared with those exerted by the motherand the environment, has been largely unexplored. Herewe used multivariate analyses to investigate the relativeimpact of maternal, environmental and social factorson offspring growth and survival in co-operativelybreeding meerkats

Suricata suricatta

, Desmarest.Meerkats are medium-sized (up to 1 kg), diurnal,

social mongooses that live in groups of two to 30 indi-viduals in arid regions of southern Africa. Groups typ-ically comprise a dominant male and female breeder(who account for the majority of pups born; Clutton-Brock

et al

. 2001b) and their retained offspring of bothsexes and various ages that act as helpers by guardingand feeding subsequent litters (Clutton-Brock

et al

.2000, 2001a). Despite being desert adapted, meerkatsare sensitive to both low and high temperatures; indi-viduals can spend up to an hour warming up beforeforaging in the mornings and often spend the middlepart of the day resting in the shade. In addition, breed-ing is dependent upon sufficient rainfall (Doolan &Macdonald 1997; Clutton-Brock

et al

. 1999). Femalemeerkats give birth to litters of three to eight pupsunderground after a gestation period of approximately70 days. Pups spend their first 3 weeks in the burrow andbegin to follow the group on foraging trips at 1 month.

Before emergence, pups may rely solely on theirmothers for milk, although in some cases allo-lactatorsmay supplement intake. In line with this, both litter sizeat birth and average weight at emergence are positivelycorrelated with the mother’s weight at conceptionand are unrelated to group size (Russell

et al

. 2002).Following emergence (and weaning), pups are typicallyprovisioned with insect larvae, arachnids and smallreptiles by all group members until independence at10–12 weeks (Doolan & Macdonald 1996; Brotherton

et al

. 2001), and the amount they are fed (biomassintake per hour) is significantly related to group size(Clutton-Brock

et al

. 2001c). We investigate what factors influence: (i) the rate of pup

daily weight gain and overnight weight loss during peakprovisioning; (ii) pup growth rates; and (iii) pup weightat, and survival to, independence. The terms tested fortheir significance in explaining variation in the above werea range of maternal (age, weight, dominance status),environmental (rainfall, temperature) and social factors(group size, number of carers per pup, carer weight gain).

Methods

Our study area is located on farmland in the South

African Kalahari, close to Van Zyls’ Rus (26

°

58

′

S,21

°

49

′

E), where dry riverbeds, herbaceous flats andsparsely grassed dunes are the typical habitat. Dataused in this study were collected between December1996 and April 2000. During this period, both temper-ature (minimum and maximum shade temperature)and rainfall were measured daily at the site; minimumtemperature refers to lowest overnight temperatureand maximum temperature to the highest daytime tem-perature during a period of 24 h. The study area experi-ences two distinct seasons (Clutton-Brock

et al

. 1999),a cold-dry season (May–September) and a hot-wet sea-son (October–April). During the cold-dry season, theminimum temperature ranged from

−

3·5

°

C to 19

°

C(mean = 6·9

°

C) and the maximum from 11

°

C to37·5

°

C (mean = 22·3

°

C), while during the hot-wet sea-son, minimum temperature ranged from 0

°

C to28·5

°

C (mean = 18

°

C) and maximum from 17·5

°

C to43

°

C (mean = 33·2

°

C). Monthly rainfall ranged from0 mm to 43 mm (mean = 5·5 mm) during the formerperiod and from 0 mm to 224 mm (mean = 45·7 mm)during the latter.

Data were collected on one to 13 breeding attempts(mean = 5·8) for eight groups of meerkats comprisingfive to 28 individuals (mean = 16·3), with a mean sizevariation of 8·1 individuals within groups and 15·2between groups. Although litter sizes at emergence var-ied from one to six (mean = 3·56), the number of pupspresent at any one time varied from one to 13 (mean =5·3) because in some cases multiple females bred. Allanimals within groups were individually identifiablefrom easily maintainable unique haircuts, completelyhabituated to very close observation (< 1 m) and over90% could be weighed repeatedly each day by enticingthem onto electronic balances using crumbs of hard-boiled egg. Group members were weighed (i) at dawn,before the initiation of foraging; (ii) at midday, at theend of the morning foraging period (3–4 h later); and(iii) at the end of the day, after cessation of foraging. Inaddition to collecting weight data for most group mem-bers, information regarding the number of pups, preg-nancy and dominance status of females, and groupsizes were also recorded (Clutton-Brock

et al

. 2001b).Group size is the number of group members excludingpups (i.e. those less than 3 months old). Because allindividuals over 3 months old are independent andpotentially contribute to feeding pups (Doolan &Macdonald 1997; Brotherton

et al

. 2001), we calculatedcarer : pup ratios as the number of group members over3 months old to the number under 3 months old. All meanspresented in the text are to

±

one standard deviation.

In this study, effects of fixed terms on continuous andnon-continuous response terms were consideredusing residual maximum likelihood (REML) modelsand iterated restricted residual maximum likelihood(IRREML) models, respectively, in GENSTAT 5·4·1


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(GENSTAT 1993) [IRREML models are a form ofgeneralized linear mixed model (GLMM)]. REML andIRREML models are similar to GLM models, withnormal and non-normal error structures, respectively,except that they allow both fixed and random terms tobe fitted (Schall 1991). Random terms took intoconsideration repeated sampling of the same indi-vidual and of different individuals within the samelitter or group. All likely maternal, environmental andsocial explanatory terms were initially entered intothese models and then sequentially dropped until themodel only included terms whose elimination wouldhave significantly reduced the explanatory power of themodel. Significantly correlated terms were neverentered into the final models together because thiswould have given rise to spurious estimations ofvariance explained. If two terms,

x

1

and

x

2

were sig-nificantly correlated,

x

2

was regressed on

x

1

, and theresiduals from this regression and

x

1

were fitted intothe model.

The significance of explanatory terms in REML andIRREML models were assessed by their Wald stat-istics, which were distributed as

χ

2

for each term fittedlast in the model. Each table presenting the results of aREML or IRREML model shows the terms added tothe model along with their Wald statistic (

χ

2

) and levelof significance under ‘model terms’. For significantterms (

P

< 0·05), statistics and probability values werederived from having all significant terms in the model,whereas the values shown for non-significant termswere derived from having all significant terms in themodel and each non-significant term in the modelindividually. For significant terms, their averageeffects and standard errors are shown under ‘minimalmodel’. The average effect of a term shows whether itsrelationship with the response term is positive ornegative after setting the lowest value (or the alphabet-ically first value for text) of that term to zero. Interac-tions are depicted by *; only the significance values ofsignificant interactions are presented and their effectsare shown graphically using the effects and the con-stant to calculate the predicted means. For interac-tions containing at least one factor, REML andIRREML outputs show the level of significance for thefirst level of each factor with an interaction only, thusby changing the order in which levels of factors areentered into the models, the significance values of eachlevel of a factor within an interaction can be obtainedwithin the overall model. In other words, univariatepost-hoc analyses were not necessary for determininglevels of significance within factors when using eitherREML or IRREML. The significance values of termscontained in interactions were obtained from runningmodels without the interactions. All response variables(REML) were normally distributed, as were theresidual plots arising from the minimal model (REMLand IRREML). Continuous and ordinal variableswere fitted to the models as variates, but see Figs 2 & 3.Discrete terms were always factorised.

An important aspect of offspring growth post-weaningis likely to be the rate at which weight is gained each dayduring the period of peak food provisioning. Weanedmeerkat pups are fed most intensively in the first 3–4 h of each day between the ages of 35 and 75 days(Brotherton

et al

. 2001). The rate at which pups gainedweight each day (hereafter referred to simply as dailyweight gain) was calculated from the rate of weightchange (grams per hour) between morning and middayweighing sessions and expressed as a percentage tocontrol for differences in initial pup weight.

To investigate which terms affect pup daily weightgain, a REML analysis was conducted using 1531morning to midday weight sequences from 137 pups in42 litters from eight groups. Because the response vari-able, daily weight gain, was expressed as a percentage, itwas normalized using arcsine square-root transfor-mation. The fixed, potential explanatory, terms fittedwere: (i) maternal characteristics (age, weight, dom-inance status); (ii) environmental characteristics(rainfall, temperature); (iii) social factors (group size,number of carers per pup, carer weight gain); and (iv)pup characteristics (weight at 1 month, age). Pupweight at 1 month was fitted to control for differentialeffects of maternal investment pre-weaning. Maternalcharacteristics were measured at conception (60–80 days prior to litter birth), while maximum tem-perature, group size, carer numbers per pup, carer weightgain and pup age were measured on the same days thatpup weight gains were obtained. Carer weight gain refersto the average percentage morning weight gain (gramsper hour) for all individuals in a group over 3 monthsold. Rainfall was measured over the previous 30 days andminimum temperature was measured over the previousnight. Individual, litter and group identities were fittedto the model as random terms to control for repeatedsampling of the same pups (1–36, mean = 11), litters(1–123, mean = 36) and groups (49–382, mean = 170).

Offspring growth and survival need not only be cor-related with the amount of weight gained per day duringpeak provisioning, but also the amount lost overnight.Overnight weight loss was calculated using the differ-ence in weight between evening and morning weighingsessions, and converted to a percentage by expressingweight loss relative to evening weight.

To investigate which terms affect overnight weight loss,a REML analysis was conducted using 1295 evening tomorning weight sequences from 195 pups in 62 littersfrom eight groups. Overnight weight loss was arcsinesquare-root transformed to ensure normality. The fixed,potential explanatory, terms fitted were: (i) maternalfactors (age, weight, dominance status); (ii) environ-mental factors (rainfall, temperature); (iii) social factors(group size, number of carers per pup); and (iv) pup


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characteristics (age, daily weight gain). Pup age anddaily weight gain (percentage weight gained betweenmorning and evening weighing sessions) were fitted tocontrol for any age-related differences in thermody-namic properties or levels of food intake. Most termsfitted in this model were obtained as described above forthe daily weight gain analysis, but minimum temperaturewas measured on the same night as the weight loss wasmeasured. Individual, litter and group identities werefitted as random terms to control for repeated measuresof the same individuals (1–29, mean = 6·6), litters (1–99,mean = 20·9) and groups (30–297, mean = 162).

Pup growth rates during peak provisioning wereobtained by regressing the age of each pup on its morn-ing weight and using the gradient of the regression linesto give an average growth rate in grams per day. Regres-sions were obtained for those pups for which greaterthan four weights had been obtained (4–27, mean =13·3 measures per pup). To investigate what factorsinfluence the growth rate of pups, a REML analysiswas conducted using the growth rates of 98 pups from26 litters in eight groups. The potential explanatoryterms fitted were: (i) maternal characteristics (age,weight); (ii) environmental factors (rainfall, temper-ature); and (iii) social factors (group size, carer numberper pup, carer daily weight change). Maternal charac-teristics were average measures at conception, andenvironmental and social factors were average meas-ures over the peak provisioning period. Daily weightchange of carers was the mean change in weight forindividuals between morning and midday weighingsessions over the same period as was measured forpups. Because, in this analysis, carer weight change wascalculated over a 40-day period (instead of a single dayas for above), only the average weight change of carersover 1 year old was used, as the weight change of thoseyounger than this is likely to reflect growth rather thanproviding an estimate of condition or food availability(Barnard 2000). Litter and group identities were fittedas random terms to control for repeated measures ofdifferent individuals within litters (1–7, mean = 3·6)and groups (3–37, mean = 12·7).

Meerkat pups begin to receive less food when 10 weeksold and are more or less fully independent at 3 months(Doolan & Macdonald 1997; Brotherton

et al

. 2001).Although meerkat pups forage independently andare rarely provisioned by helpers after 3 months, notevery individual was weighed at 3 months precisely. Pre-foraging weights (

n

= 584) obtained for 87 individualsbetween 91 and 120 days old were used to determineweight at independence.

A REML analysis was conducted using the meanweights for 87 individuals from 34 litters in eight

groups. The factors fitted were: (i) maternal factors(age, weight, dominance status); (ii) environmental fac-tors (rainfall, temperature); (iii) social factors (groupsize, carer numbers per pup); and (iv) pup character-istics (average age at weighing, weight at 1 month, dailyweight gain, overnight weight loss). Maternal, environ-mental and social factors were measured as describedabove in the growth analysis. Pup weight gain andovernight weight loss were average values for pupscalculated over the period of peak provisioning. Pupweight gain was the average absolute (not the per-centage) age-related weight for each pup. Litter andgroup identities were fitted as random factors tocontrol for repeated measures of different individualswithin the same litters (1–5, mean = 2·6) and groups(2–32, mean = 10·8).

Pup survival was measured as the proportion of pupssurviving from 35 days (approximate age of weaning)to 90 days (approximate age of independence). Usingtwo IRREML analyses, we investigated the effects onsurvival of: (i) maternal, environmental and social fac-tors (see above); and (ii) pup characteristics (pup age-related weight at 1 month and average pup weight gainand weight loss during peak provisioning). Pup age-related weight at 1 month is likely to reflect maternalinvestment (Russell

et al

. 2002). Maternal characteristicswere measured at conception, and environmental andsocial factors were the average values for each individualcalculated between 35 days and either independenceor death (whichever came first). The analyses, on 175pups from 52 litters in eight groups, were conductedby fitting the survivorship data to a binomial errordistribution with logit-link function. Repeated measureswithin litters (1–6, mean = 3·4) and groups (7–46, mean= 21·8) were controlled by fitting litter and groupidentities as random terms in the model.

It was necessary to divide the survivorship analysisinto these two separate analyses because the low levelsof pup mortality found during this study meant that thenumber of degrees of freedom was insufficient to testthe significance of all terms in a single model. It isacknowledged that such an approach is not ideal, butas tests with different combinations of the independentterms in each model yielded similar results, it issuggested that this approach is not likely to have givenrise to spurious findings. However, because the degreesof freedom from such an approach will be increased,marginally significant terms or obviously correlatedterms should be viewed with caution.

Results

Weaned pups gained on average 1·4% of their bodyweight per hour (range = 0·25–4·4%) during each


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morning of their period of peak provisioning (35–75 days old). Pup daily weight gain post-weaning wasprimarily influenced by social and environmental factors(Table 1). Daily weight gain was positively influencedwhen the ratio of carers to pups was high and whencarers themselves showed relatively high rates of weightgain. The percentage weight gain of carers averaged0·87 g h

−

1

(range 0·15–1·6 g h

−

1

), equalling 5·2 g h

−

1

inabsolute terms (range 0·96–12·6 g h

−

1

). Carer weightgain was positively correlated with previous month’srainfall (

F

1,49

= 5·23,

P

= 0·027) and daytime temper-atures (

F

1,49

= 10·79,

P

= 0·002). Independently of theseeffects, pups born to subordinate mothers showedlower rates of weight gain on days when daily tem-peratures were high (Fig. 1a), and higher rates of weightgain when rainfall was high (Fig. 1b).

On average, pups lost 4·6% of their body weight over-night (range = 1·3–8·6%). Overnight weight loss wasprimarily influenced by characteristics of the pups andthe overnight temperatures they experienced (Table 2).Old pups and those gaining a large percentage ofthe body weight over the course of a day lost a greaterpercentage of their body weight overnight. Aftercontrolling for these effects, overnight weight loss wasalso found to be influenced by low overnight temper-atures. The negative effect of low overnight temper-atures on pup overnight weight loss was less for thosepups present in large groups than for those present insmaller groups (Fig. 2).

Table 1. REML model showing the terms associated with the percentage daily weight gain of pups during peak provisioning post-weaning (i.e. between 35 and 75 days old). †Carer daily weight gain controlling for effects of rainfall and maximum temperatures.‡Rainfall controlling for effect of maximum temperature. §Minimum temperature controlling for effect of maximumtemperature. Neither pups nor groups (P > 0·5) constituted significant random terms in the model; however, there was significantrepeatability of litters (P < 0·01)

Model terms Wald statistic (χ2) d.f. P

Carer daily weight gain (g h−1)† 92·01 1 < 0·0001Number of carers per pup 11·35 1 0·001Maternal dominance status 6·57 2 0·037Maternal status * monthly rainfall‡ 8·83 2 0·011Maternal status * maximum temperature 7·80 2 0·020Pup age 2·58 1 0·11Pup weight at 1 month 2·38 1 0·13Monthly rainfall 1·01 1 0·32Maternal age-related weight 0·88 1 0·35Minimum temperature§ 0·81 1 0·37Maximum temperature 0·62 1 0·43Maternal age 0·53 1 0·44Pup sex 0·46 1 0·50Group size 0·30 1 0·59

Minimal model Average effect SE

Constant 0·095 0·0050Carer daily weight gain (%g h−1) 1·83 0·19Number of carers per pup 0·0023 0·00068Maternal status (subordinate < dominant) −0·014 0·0061

Fig. 1. (a) Maternal dominance status and rainfall effect onpup daily weight gain. Pups of dominant mothers do similarlywell in levels of low and high rainfall (χ2 = 0·66, d.f. = 1, P =0·42), pups of subordinate mothers do significantly betterin levels of high rainfall (χ2 = 6·21, d.f. = 1, P = 0·013).(b) Maternal dominance status and maximum daytimetemperature effect on pup daily weight gain. Pups born todominant mothers appear less adversely affected by highdaytime temperatures (χ2 = 0·46, d.f. = 1, P = 0·50) than pupsborn to subordinate mothers (χ2 = 4·55, d.f. = 1, P = 0·033).


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Over the period of peak provisioning, pups gained anaverage of 3·15 g 24-h period

−

1

(0·4–5·6 g). Pup growthrates were unaffected by maternal characteristics.Instead, social factors had the greatest impact on pupgrowth rates, with those pups being raised in groupswith high carer to pup ratios and during times when thecarers themselves were likely to be in good conditionhaving the fastest growth rates (Table 3). However,high daytime temperatures had a negative effect onpup growth rates.

By the time pups were independent (3–4 months old)

they averaged 344 g (range = 228–454 g). Individualweight over this period was age-related (Table 4). Aftercontrolling for the effects of age, weight at inde-pendence was found not to be affected directly by anymaternal characteristic, but was influenced by pup weightat 1 month, a correlate of maternal weight (Russell

et al

. 2002). In addition, pup weight at independencewas related positively to average daily weight gain andnegatively to average overnight weight loss during theperiod of peak provisioning.

Of the 175 pups that were weaned, 89% survived toindependence. Survival from weaning to independencewas influenced by the dominance status of a pup’smother, its sex and its level of overnight weight loss.Pups born to dominant mothers were more likely tosurvive than those born to subordinate mothers,females were more likely to survive than males, andthose losing a low percentage of their body weightovernight were more likely to survive than those losinga high percentage of their body weight overnight(Table 5). There was also a trend for those pups thatwere heavy at 1 month to survive better to independ-ence than those that were light. However, factors otherthan those directly associated with the pups themselvesstill appeared to influence survivorship (Table 6).Survivorship, independently of weight gain, increasedsharply in groups of five to 19 carers, before decliningagain, and this decline was especially pronouncedwhen maximum daytime temperatures were high(Fig. 3). In addition, pups experiencing high rainfallwere less likely to die before independence than thoseexperiencing low rainfall.

Table 2. REML model showing the terms associated with percentage weight lost by pups each night during peak provisioning.†Maximum temperature controlling for effect of minimum temperature. ‡Number of helpers per pup controlling for effect ofgroup size. Neither pups nor groups (P > 0·5) constituted significant random terms in the model; however, there was significantrepeatability of litters (P < 0·01)

Model terms Wald statistic (χ2) d.f. P

Pup daily weight gain (%) 643·97 1 < 0·0001Pup age 145·88 1 < 0·0001Minimum temperature 10·75 1 < 0·001Minimum temperature * group size 16·69 2 < 0·001Pup sex 2·41 1 0·12Group size 2·34 2 0·31Maternal dominance status 0·68 1 0·41Maternal age-related weight 0·56 1 0·45Maternal age 0·14 1 0·71Maximum temperature† 0·09 1 0·76Number of carers per pup‡ 0·01 1 0·91


Constant 0·21 0·0039Pup weight gain 0·77 0·031Pup age 0·0010 0·000083Minimum temperature −0·0012 0·00027

Fig. 2. Group size and minimum overnight temperatureeffect on pup overnight weight loss. At high temperatures,group size has little effect on overnight weight loss (χ2 = 1·21,d.f. = 2, P = 0·47) but at lower temperatures increases in groupsize are associated with significant reductions in weight loss(χ2 = 15·57, d.f. = 2, P < 0·01).


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Discussion

Analyses of the factors influencing litter size at birthand weight at 1 month in the same population of meer-kats show that maternal characteristics are of primaryimportance for both variables (Russell

et al

. 2002). Incontrast, maternal characteristics have little directinfluence on pups after weaning, although pups bornto subordinate females have lower rates of weight gainand survival than those born to dominants. Instead,environmental and social factors primarily influencepups after emergence, with both significantly influen-cing pup daily weight gain, growth, overnight weightloss and survival. However, maternal investment

pre-weaning does translate into weight differencesamong pups at independence. Thus, in co-operativelybreeding meerkats, social factors primarily, but notwholly, replace the importance of the maternal charac-teristics that commonly govern reproductive successin non-co-operatively breeding social species.

The daily weight gain and growth of pups followingweaning were primarily related to the number of carersper pup and the daily weight gain of those carers. Thisis presumably because pups are fed more in the presenceof many well-fed helpers; experimental manipula-tions of helper : pup ratios influence pup weight gain(Clutton-Brock

et al

. 2001c), and manipulations ofhelper condition affect contributions to pup feeding

Table 3. REML model showing parameters associated with pup growth during peak provisioning. Pup growth represents themean change in weight each day between the ages of 35 and 75 days. †Carer weight change after controlling for effects of numberof carers per pup and maximum temperature. ‡Rainfall controlling for effect of maximum temperature. There was significantrepeatability within litters (P < 0·05), but not groups (P > 0·5)

Model term Wald statistic (χ2) d.f. P

Number of carers per pup 6·98 1 0·005Maximum temperature 5·29 1 0·015Carer weight change† 4·77 1 0·022Group size 2·98 1 0·085Pup sex 0·94 1 0·33Monthly rainfall‡ 0·91 1 0·34Maternal age-related weight 0·83 1 0·41Maternal age 0·47 1 0·69


Constant 3·088 0·15Number of carers per pup 0·24 0·087Maximum temperature −0·062 0·026Carer weight change 0·20 0·086

Table 4. REML model showing terms associated with weight at independence (between 3 and 4 months). †Overnight weight losscontrolling for daily weight gain. There was significant repeatability within litters (P < 0·05) but not groups (P > 0·5)


Pup age at weighing 17·35 1 < 0·001Pup daily weight gain (g h−1) 9·27 1 0·002Pup weight at 1 month 6·17 1 0·013Pup overnight weight loss† (%) 4·40 1 0·036Monthly rainfall 1·94 1 0·16Maternal status 2·47 2 0·29Maternal age 0·78 1 0·38Number of carers per pup 0·66 1 0·42Minimum temperature 0·43 1 0·52Maternal age-related weight 0·40 1 0·53Maximum temperature 0·03 1 0·85Group size 0·01 1 0·97Sex 0·01 1 0·97


Constant −12·32 11·11Pup age at weighing 14·36 2·97Pup weight at 1 month 0·46 0·11Pup daily weight gain 11·70 3·89Pup overnight weight loss (%) 6·36 3·03

JAE_636.fm 06 Tuesday, July 2, 2002 9:25 AM

707Growth and survival of meerkat pups

© 2002 British Ecological Society, Journal of Animal Ecology, 71,700–709

(Clutton-Brock et al. 2001a). These findings are import-ant for two reasons. First, the daily weight gain of pupsduring peak provisioning had a significant effect ontheir weight at independence, and weight at independ-ence has been shown to correlate with weight through-out an individual’s first year of life (Clutton-Brock et al.2001c). Secondly, in their first year of life, individualsthat are heavy for their age may contribute more toco-operative activities than those that are light for theirage (Clutton-Brock et al. 2000).

Neither maternal weight nor age had any directinfluence on offspring daily weight gain or growthpost-weaning, but daily weight gains of pups born tosubordinate females were lower than those born todominant females. This is surprising given that helpersdo not appear to feed preferentially the pups of dom-inant females (Clutton-Brock et al. 2001a). One pos-sible explanation is that most pups born to subordinatemothers have to compete with older more dominantpups, while this is not the case for the latter, which areeither born and raised in the absence of competingpups, or are older and more dominant than their

competitors (Clutton-Brock et al. 2001b). The factthat pups born to subordinates gain significantly moreweight per hour when rainfall is high (and food is likelyto be more plentiful; Doolan & Macdonald 1996, 1997;

Table 5. IRREML showing the pup characteristics associated with survival from emergence to independence. There wassignificant repeatability within litters (P < 0·05) but not groups (P > 0·5)


Maternal status 128·67 1 < 0·0001Overnight weight loss (%) 18·05 1 < 0·001Pup sex 4·57 1 0·035Pup weight at 1 month 3·30 1 0·069Daily weight gain (%) 2·24 1 0·12

Minimal model Average effects SE

Constant 5·14 0·77Maternal status (subordinate < dominant) −5·68 1·062Overnight weight loss (%) −135·0 31·78Pup sex (males < females) −1·18 0·55

Table 6. IRREML showing the maternal, social and environmental characteristics associated with pup survival from emergenceto independence. †Rainfall controlling for effect of maximum temperature. There was significant repeatability within litters(P < 0·05) but not groups (P > 0·5)


Maximum temperature 18·44 1 < 0·001Monthly rainfall† 12·44 1 < 0·001Group size * maximum temperature 8·60 2 0·014Group size 7·27 2 0·026Number of carers per pup 1·47 1 0·13Maternal age 0·91 1 0·34Maternal age-related weight 0·19 1 0·67

Minimal model Average effects SE

Constant 1·24 1·38Maximum temperature −0·49 0·11Group size < 12

12–19> 19

0 04·92 1·981·73 1·79

Rainfall 0·070 0·020

Fig. 3. Group size and maximum daytime temperatureeffects on pup survival between weaning and independence.Although group size initially offers survival benefits to pups(χ2 = 17·99, d.f. = 1, P < 0·001), pup mortality increases ingroups over 19 individuals and this is especially the case whendaytime temperatures are high (χ2 = 9·91, d.f. = 1, P < 0·002).


708A. Russell et al.


Barnard 2000), and gain significantly less weight whendaytime temperatures are high and begging is energet-ically more demanding, supports this suggestion.

Overnight weight loss had consequences for bothpup weight at, and survival to, independence. Over-night weight loss of pups increased when overnighttemperatures were low, and this effect was especiallystrong in small groups. The probable explanation is thatmembers of meerkat groups sleep together in a singlechamber, with the result that large group sizes mediatethe effects of low temperatures on pup weight loss.Mediation of low temperatures on energy expenditureor weight loss has been suggested to be an importantselective force behind communal living in many co-operative breeding birds and mammals (Riehm 1970;Arnold 1990; Williams, Du Plessis & Siegfried 1991).

Pup weight at independence was influenced by bothdaily weight gain and overnight weight loss during theperiod of peak provisioning. Weight at or near inde-pendence is known to have long-term fitness conse-quences in meerkats (Clutton-Brock et al. 2000, 2001c)and other co-operative breeders (Hatchwell 1999).Factors that are associated with increasing daily weightgain and reducing overnight weight loss are thereforelikely to be under selection. Because daily weight gainaffected weight at independence more significantlythan overnight weight loss, factors affecting the formerare likely to be under stronger selection than thoseaffecting the latter. However, factors acting duringpeak provisioning do not wholly replace the import-ance of maternal investment pre-weaning, as pups thatwere heavy at 1 month were heavy at independence.

Pup survival between emergence and independencewas influenced by social, maternal and environmentalfactors. Although offspring starvation is common inco-operative breeders, it is not universal (Hatchwell1999) and does not constitute a major form of mortal-ity in meerkats. A significant source of pup mortalityin meerkats, in addition to predation (Doolan &Macdonald 1997; Clutton-Brock et al. 1999b), is beingdetached from the group when tired (T.H. Clutton-Brock, unpublished data). Three lines of evidence sup-port this. First, despite carer weight gain increasingwith daytime temperatures, pup daily weight gain andgrowth were negatively associated with high day-time temperatures. Secondly, pups born to subordinatemothers and those that were male had relatively lowsurvivorship; pups born to subordinates are youngerand less able to remain with the group than older pupsborn to dominants (Clutton-Brock et al. 2001a), andmale pups do not remain in such close contact to groupmembers as female pups (Brotherton et al. 2001).Finally, pup mortality is lower during periods of highrainfall probably because prey abundance is higher(Doolan & Macdonald 1997; Barnard 2000) andgroups have to travel less far for food.

Pup survivorship showed a bell-shaped distributionwith group size. Although Brown (1987) suggestedsuch distributions should occur in co-operative breed-

ers, they have not been shown before in obligate species.The reasons why pups are more likely to becomedetached in large groups are two-fold. First, the greatergroup dispersion found in large groups (Barnard 2000)results in pups travelling further between group mem-bers for food and tiring more rapidly. The finding thatpup mortality is highest in the largest groups when day-time temperatures are high supports this conjecture.Secondly, because per capita contributions to pup feed-ing and residual benefits from increasing pup survivor-ship are low in very large groups, carers appear lessresponsive to missing pups and their distress calls (T.H.Clutton-Brock, unpublished data).

In summary, by helping, individuals increase theweight and number of pups surviving to independ-ence. This is likely to benefit helpers indirectly,because groups chiefly comprise relatives, and directly,as increases in group size afford survival benefits(Clutton-Brock et al. 1999). In addition, because weknow that weight at independence is correlated with anindividual’s weight (Clutton-Brock et al. 2001c) andcontribution to helping (Clutton-Brock et al. 2000)throughout its first year of life, by helping to raise thesize and quality of the workforce, helpers are likely togain delayed benefits by being able to reduce theirinvestment in helping in the future. A delayed benefit ofthis kind to helping has seldom been considered buthas important implications for the direct component offitness calculations of a helper’s inclusive fitness. There-fore, although offspring survival need not translateinto fitness gains for helpers, because breeding is not anautomatic by-product of survival, in a family-living co-operative breeder where reproductive success is largelygoverned by helper investment and helper investment iscondition dependent, it is probable that any factor thataffects pup survival and condition will affect breederand helper fitness both directly and indirectly.

Studies of co-operative breeders frequently showthat helpers improve the condition and/or survival ofthe offspring they help to raise (Emlen 1991; Jennions& Macdonald 1994; Cockburn 1998). This study pro-vides a mechanism for such correlations by showingthat, through their influence on rates of daily weightgain and growth, helpers improve the weight of pups atindependence; and, through their ability to reduceovernight weight loss and increase predator detection,they help to reduce pup mortality. The magnitude ofsuch helper effects is generally considered by compar-ing reproductive success for the same individuals withvarying numbers of helpers (Emlen 1991). However,this approach is questionable given that mothers candifferentially invest in their offspring depending onpotential fitness returns (Cunningham & Russell 2000).By considering reproductive success independently ofmaternal investment, we are able to show the magni-tude of helper effects independently of any potentialconfounding influence of differential maternal invest-ment. Finally, to our knowledge, studies have not pre-viously considered the relative importance of maternal,


709Growth and survival of meerkat pups


environmental and social effects on reproductive successfor a co-operatively breeding vertebrate in the samemultivariate analyses. This study shows that inter-actions between environmental and social factors arelikely to exert the strongest selection in co-operativebreeders, but that selection on maternal effects is alsosignificant. Thus, in the meerkat, social factors largely,but not wholly, replace the importance of maternalcharacteristics for reproductive success that are commonlyshown in non-co-operatively breeding social species.

Acknowledgements

We are indebted to Mr and Mrs H. Kotze for allowingthis work to be carried out on their land, to MartinHaupt and Johan du Toit at the University of Pretoriaand Penny Roth at Cambridge for logistical help withthe project, and to the many volunteers, students andpost-docs who contributed to data collection. Thispaper has benefited from the help, advice and/orcomments of Tim Coulson, Jason Gilchrist, JaniLindström, Anne Carlson, Sarah Hodge and oneanonymous referee. This study was funded by theNatural Environmental Research Council and Biotechno-logy and Biological Sciences Research Council, forwhich we are grateful.

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Received 15 October 2001; final copy received 15 March 2002


factors affecting pup growth and survival in co-operatively breeding meerkats suricata suricatta

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