band structure and failures of reproductive …...maurice calvert-evers and john elford of nissan...

BAND STRUCTURE AND FAILURES OF REPRODUCTIVE

SUPPRESSION IN A COOPERATIVELY BREEDING

CARNIVORE, THE SLENDER-TAILED MEERKAT (SURICATA

SURICATTA)

by

SEAN P. DOOLAN1) and DAVID W. MACDONALD2,3)

(Wildlife Conservation Research Unit, Department of Zoology, South Parks Road, Oxford OX1 3PS, UK)

(Acc. 11-II-1997)

Summary

The extent to which band structure influences the distribution of breeding activity is unknown for the slender-tailed meerkat Suricata suricatta, a cooperatively breeding mongoose. Here we present the residence histories of three focal bands monitored over ten band-years in the southwestern Kalahari, with less detailed data derived from non-focal bands for a further 20 band-years. Mean total band size early in the breeding season was 10, and mean

1) Present address: Earthwatch Europe, Belsyre Court, 57 Woodstock Road, Oxford OX2 6HJ, UK; e-mail: [email protected] 2) Corresponding author. 3) We gratefully recognise the permission of Mnr. Elias Leriche and the Trustees of the National Parks Board of South Africa to work in the KGNP. Many people contributed additional observations on meerkats, including Maans Dreyer, Mike and Anette Knight, Colin Sapsford, David Paynter, Richard Goss, Steve Giddings, Barry Lovegrove, and Koetie Herholdt. SPD thanks Dorcas Walker for enduring the completion of this work and Karen Wiltshire for support in the field, not to mention the support band at the 39 steps. This study forms part of a PhD thesis by SPD, who was financially supported by the Royal Commission for the Exhibition of 1851, an Anglo-Irish Scientific Scholarship, a Wolfson College graduate award and the Prendergast Trust of the University of Oxford. Part of the work was conducted while DWM was a visiting research fellow at the Mammal Research Institute of the University of Pretoria, where the hospitality of Prof. John Skinner and the support of the CSIR are warmly acknowledged. Maurice Calvert-Evers and John Elford of Nissan S.A. provided vehicles at key periods. We thank Claudio Sillero-Zubiri, Scott and Nancy Creel, Rosie Woodroffe, Gus Mills and especially Fran Tattersall for discussion and input to earlier versions of this manuscript.

Downloaded from Brill.com02/06/2020 02:22:26AMvia Arizona State University

828

size excluding juveniles was 6.7. Despite a tendency towards females among juveniles, and males among yearlings and adults, sex ratios within each age class did not significantly deviate from unity, but at the population level there were significantly more adult males than reproductive females. A large proportion (71.6%) of adult females bred, and failures of reproductive suppression occurred in 40% of band years. This incidence was high in all

years and was not obviously related to environmental conditions. Bands with more than one reproductive female contained significantly more adults and adult females than bands with only a single reproductive female. There was a strong correlation between numbers of reproductive females and numbers of adult females in a band. Most (68%) subordinate females which bred were aged three years or more. Reproductive competition was

strong and there was a negative correlation between numbers of adult females, breeding females or adult males and per capita juvenile production. Meerkat bands are unusual

among cooperative breeders because many individuals were non-kin and the relative con-

stancy in band size within and between years masked a high turnover of membership: all animals of known origin aged three years or older, were immigrants, although philopatry was commoner among younger animals. Our data show that meerkats employ a range of

reproductive strategies: bands exhibiting a spectrum of reproductive suppression coexist, and individuals respond to the opportunities afforded by their social environments.

Keywords: Suricata suricatta, meerkat, mongoose, cooperative breeding, reproductive suppression, group structure, demography.

Introduction

Group structure, demography and social relationships between individuals

are closely interlinked (Altmann & Altmann, 1979; Dunbar, 1979). Group

structure is dynamically determined by social and kin relationships, and

also by demographic processes operating under the influence of ecologi-

cal conditions (Robinson, 1988a, b). The distribution and availability of

potential social partners provides the backdrop against which individuals

play out their social and reproductive strategies (Emlen & Wrege, 1994).

Consequently, both the ability of an individual to acquire rank and breed-

ing position, and the fitness returns yielded by kinship patterns (Creel &

Waser, 1991, 1994), are modified by group composition (Dunbar, 1989).

Data on group structure are particularly relevant to understanding cooperative breeding since ecological and demographic conditions can constrain

reproductive and dispersal opportunities, and thereby promote conditions

favouring cooperation (Macdonald & Carr, 1989; Emlen, 1991; Koenig

et al., 1992). For example, a skewed sex-ratio can limit breeding opportunities for the more abundant sex, creating a pool of potential helpers


829

(Malcolm & Marten, 1982; Russell & Rowley, 1993). High levels of re-

productive investment may constrain independent breeding and favour the

accumulation of helpers in a positive feedback loop (Creel & Creel, 1991;

Creel & Macdonald, 1995). Changes in ecological conditions may act to

increase or decrease the magnitude of constraints, effectively creating win-

dows of opportunity when the costs of reproduction are diminished or the

likelihood of successful dispersal or breeding is increased (Emlen, 1991).

In this way, dominant Galapagos mockingbirds Nesomimus parvulus recruit

the support of helpers in dry years by interfering with the breeding attempts of subordinates (Curry, 1988) whilst changes in demographic structure can

allow more yearlings to breed in other years (Curry & Grant, 1989). Alter-

natively, direct benefits of philopatry such as access to critical resources,

reduced predation risk from group membership, or increased likelihood

of territory inheritance may predispose individuals to remain in their natal

groups (Ligon et al., 1991; Stacey & Ligon, 1991). Potential indirect fitness

gains for helpers are greatest when they assist close relatives, and decline

with a decrease in the coefficient of relatedness (Koenig et al., 1992). Both

direct and indirect gains must be set against the costs of remaining in a

group (e.g. foraging or reproductive competition), and the potential gains to be made from dispersal and breeding in other groups.

Cooperatively breeding species are often classified as plural breeders

(in 'egalitarian' societies in which most or all females breed), and singular breeders (in 'despotic' societies in which only a primary or dominant

female breeds and subordinates are reproductively suppressed) (Vehren-

camp, 1983; Brown, 1987; Emlen, 1991). However, these represent the

extremes of a spectrum of reproductive strategies (Keller & Reeve, 1994).

Vehrencamp's (1983) model predicts that reproductive suppression should

be most pronounced when: (1) indirect fitness accrued by subordinates

through helping is substantial; and (2) independent breeding opportunities for subordinates are limited. Indirect fitness is influenced by kinship patterns within groups, and by the effectiveness of help in augmenting the

dominant's reproductive success, whilst the degree of leverage exerted by the dominant is strengthened by risky dispersal and low turnover of repro- ductives (Waser et al., in press).

Most cooperatively breeding carnivores (13 of 17 species) exhibit re-

productive suppression of subordinates (Macdonald & Moehlman, 1983;


830

Keane et al., 1994; Creel & Macdonald, 1995). Classification schemes

and comparative analyses emphasise species-typical patterns of social or-

ganization (e.g. Bekoff et al., 1984; Gittleman, 1985, 1989; Packer, 1986;

Rood, 1986) and tend to overlook the variability within complex societies.

However, the circumstances surrounding failures in reproductive suppression can reveal more about the fitness decisions made by individuals than

broad species-level generalisations. Slender-tailed meerkats (Suricata suricatta) are gregarious cooperative

breeders. All band members, both male and female, assist breeding ani-

mals by babysitting at the den and provisioning young on foraging trips

(Doolan, 1994) during the breeding season from October to June (Doolan & Macdonald, in prep.). However, little is known of the extent to which

reproductive suppression occurs, or of how this relates to band structure

(Lynch, 1980; Roberts, 1981 ). Given the ecological parallels (Rood, 1986;

Waser et al., in press), one would expect the demography and social or-

ganization of meerkats to be similar to other gregarious mongooses. Here

we outline the residence histories of individuals within three focal bands of

meerkats in the southwestern Kalahari over a period including wet and dry

years. We then consider the relationships between band structure, indices

of per capita reproductive success and failures of reproductive suppression.

Methods

Study area

The study was conducted near Nossob camp (25°25'S, 20°36'E) in the Kalahari Gemsbok National Park, South Africa and Gemsbok National Park of Botswana. The study area was

composed of open Kalahari thornveld (Acocks, 1988), with rolling sand dunes and river terraces bordering onto the dry bed of the Nossob river (Doolan, 1994). The region is semi- arid, and experiences erratic rainfall with wide daily and seasonal temperature variation. The hot, wet summer (when almost all rains fall, and mean monthly temperatures exceed 20°C) runs from October to April and the cold, dry winter (mean monthly temperatures below 20°C, accompanied by occasional ground frosts and nocturnal temperatures as low as -10°C) runs from May to September (Leistner, 1967). Over the duration of the study, 1985/'86 was exceptionally dry but heavy rains fell in 1987/'88 (Doolan & Macdonald, 1996a).

Data collection and analysis

This paper presents a record of the dynamics of three focal meerkat bands (Raiders, Wood- landers and Outliers) over four, four and two breeding years (October to September), re-


831

spectively, giving a total of ten band years between 1984/'85 and 1987/'88. The data are

initially presented as band histories. Major behavioural events accompanying changes in band membership are outlined qualitatively in order to establish a social context. The data are then summarised across all bands.

Except for when young are being guarded at the den, meerkat bands forage together cohesively throughout the day (Roberts, 1981; Doolan & Macdonald, 1996a). Complete counts of all band members were readily carried out at sleeping dens. For each band we recorded all pregnancies, births, deaths, immigrations, emigrations, unexplained disappear- ances, and the presence of transients. Immigration occurred when a band was joined by an outsider for at least four weeks. Band size was determined from counts made in January (prior to most births) and July (at the end of the breeding season) of each year. Focal bands were well habituated and were observed from dawn to dusk on foot at a distance of several metres. All individuals in focal bands were identifiable by scars, and by pelage and behavioural characteristics. A total of 125 individuals were monitored within the focal bands over the period reported here. More extensive data on demography and the distribution of reproductive activity within bands were gathered by intermittent observations on the composition of 2-8 other bands, yielding data for an additional 20 band years. Only bands for which complete counts were available were included in the data set reported here. Unhabituated meerkats were observed through binoculars from a vehicle.

Animals were allocated to three age classes, defined in terms of the number of winters

(dry seasons) following an individual's birth (Rood, 1990). Juveniles had not yet survived a winter. Yearlings were between their first and second winters, during which time they attain sexual maturity (Ewer, 1963; Lynch, 1980). Adults were animals which survived

through a second winter. Body size, and relative development of muscular ridges on the crown of the head and above the brows permitted identification of age classes in the field (Doolan, 1994). No sexual dimorphism was apparent within the age classes or for adults and yearlings combined, but animals could be sexed visually by the scrotal sac. Dominance status was determined from ad libitum observations of social interactions and scent marking activity. The relative status of animals was readily discernible from the 'low creep' greeting and 'creep-groom' allogrooming displayed by subordinates towards dominants, whist dominant males were most active in scent marking (Doolan, 1994). With the exception of highly aggressive attacks on individuals coinciding with mating periods and dispersal events (Doolan & Macdonald, 1996b, in press), agonistic interactions were rare and of low intensity. Per capita reproductive success was calculated from the number of juveniles reared to the end of the breeding season in July.

Statistical tests for parametric and non-parametric analyses follow Sokal & Rohlf (1981). Data are presented as means 3= one standard deviation and sex ratios are reported as the

proportion of males within samples. Sample sizes differ between analyses because of

varying degrees of completeness in the data sets.


832

Results

Residence histories

The residence histories of all meerkats observed as residents within the

three focal bands between October 1984 and July 1988 are illustrated in

Figs 1 to 3. Individuals which trailed bands are not included. The histories

indicate that there is a high rate of turnover of animals within bands, with

both males and females immigrating and emigrating, and many yearlings and adults disappearing, apparently to emigrate (Doolan & Macdonald,

1996b). Up to three females were reproductively active within a band

simultaneously. Each reproductive female generally made several breeding

attempts within a breeding season although reproductive success was highly variable between years and between individuals (Doolan & Macdonald, in

press).

Adult and yearling males

Of the three adult males present in the Raiders in October 1984, only one

was still resident in July 1988 (Fig. 1). Male 02, known to be resident in

1982 (DWM, pers. obs.), remained as the dominant male for the period re-

ported here, a breeding tenure of at least 48 months. Male 01 disappeared between September and December 1985, while male 12 emigrated over the

same period, presumably in coalition with females 06 and 51. During a

period of high aggression in November 1986 which coincided with mat-

ing activity within the band, male 03 emigrated with two younger males

(04 and 16) in a takeover of the adjacent Woodlanders band and ousted

Fig. 1. Band composition and residence histories for individual meerkats in the southwestern Kalahari - the Raiders band, October 1984 to July 1988. Identities given as code numbers and names to cross-reference with other publications. Key: Horizontal lines represent individuals through time. Age classes indicated with identity at first appearance within the band. Heavy lines represent males, double lines females. Litters and offspring are connected to their mothers. Presumed matrilineal descent or identity within the band are indicated by broken lines. Periods of absence from the field are indicated by shading, and presumed presence within the band is indicated by a single line. * = death, D = disappearance, I = immigration (source band), E = emigration (target band), J = juvenile, Y = yearling,

Ad = adult.


833


834


835

the resident males (see also Doolan & Macdonald, 1996b). Two yearlings

(25 and 26) which trailed the Raiders soon after the split were actively

groomed by male 02 upon their initial appearance. Both joined the Raiders

but only male 26 remained for the duration of the study. Male 03 became the new dominant in the Woodlanders. He was still

present as the dominant male in February 1989, a tenure of 27 months

(D. Paynter, pers. comm.). Males 04 and 16 remained in the Woodlanders

for a year, but both dispersed independently in February 1988 and were

relocated in an adjacent band three months later. There were no other male

immigrations into the Woodlanders.

The Outliers underwent considerable turnover between their initial loca-

tion in May 1986 and January 1987. Four adult males were present origi-

nally, one an emigrant from the Raiders (male 12 = male 43). Aggression was heightened during the mating period in November 1986, and for the

next two months the band was in a constant state of flux. Both males

and females were targets of episodic aggression (sensu Vick & Pereira,

1989) initiated by a single adult female (06) and in which all animals

participated. During this interval all of the males were ousted and three

immigrant males (two adults and a yearling) were recruited. Two of the

original males (44 and 46) successfully rejoined the band with the immi-

grant males 47 (a young adult) and 48 (a yearling). Male 44 occupied the

dominant position for the ensuing two breeding seasons. Two yearlings

(78 and 79) joined the band early in 1987/'88. Males 47 and 46 made two

attempts to takeover adjacent bands in 1988, one attempt in coalition with

male 78. Another yearling male immigrated in July 1988, while male 79

was last seen trailing an adjacent band.

Adult and yearling females

The band histories also reveal that the female membership of groups is

subject to change. An immigrant to the Raiders (adult female 14) was

killed by a martial eagle in June 1985 whilst the original breeding female

(10) disappeared and presumably died during the winter of 1984/' 85. Five

Fig. 2. Composition of the Woodlanders band and residence histories for individual meerkats, April 1985 to July 1988. Key as for Fig. 1.


836


837

yearling females disappeared between September and December. The two-

year old (06) also disappeared at this time and transferred to the Outliers

with female 51 and male 12, prior to May 1986. Two young adult females

(23 and 24) were present by January 1986 although their relative rank order

was not evident during that breeding season. By the following year female

24 was the dominant of the two and female 23 was temporarily ousted

early in 1988. This aggression again corresponded to the mating period. One other two year old female (29) also joined the group between August and December 1987.

The dominant female in the Woodlanders disappeared, and probably died, between April and September 1986. Three adult females were present in

1986/' 87 after the takeover by the coalition of male Raiders, but females 60

and 62 disappeared between July and December 1987. Thus, only female

61, initially present as a two-year-old in May 1985, remained for all four

breeding seasons.

As already noted for the Outlier males, there were also considerable

changes amongst the adult females early in the breeding season of 1986/'87.

No juveniles were present when the group was initially located in May

1986, so the identity of the breeding female could not be determined. At

that stage four adult and yearling females were present, and a further two

joined in July 1986. Subsequent events suggested the loss of a dominant

female during the previous breeding season. By September 1986 only four

adults remained. During the next oestrus period in mid-November, there

was a succession of severe attacks on female 40 by female 06. The two

other younger adult females were also targeted, although to a lesser extent.

During the conflict between female 06 and female 40 a group of five male

intruders began to trail the Outliers. After a particularly aggressive attack

during which she was severely bitten, female 40 temporarily joined these

males. She rejoined the Outliers but later the same afternoon she left with

the other two females and surreptitiously travelled after the intruders. By late December 1986 all three of the dispersers were back in their original home range, although female 40 was by then allied with the males 43

Fig. 3. Composition of the Outliers band and residence histories for individual meerkats, May 1986 to July 1988. Key as for Fig. 1. Note that immigrant male 12 and female 51

from the Raiders are referred to as male 43 and female 42.


838

(= 12), 44 and 46, whilst females 42 (= 52) and 41 were together with

female 06 and two young immigrant adult males. A series of daily attacks

ensued over the following three weeks, both within and between the sub-

groups, during which animals changed from one sub-group to the other.

When membership had stabilised by mid February 1987, female 06 was

the only adult female remaining. There were no subsequent changes in

female membership.

Focal band size and composition

Mean total band size in January was (range: 6-15; N = 9 focal

band-years); when juveniles were excluded mean band size was 6.7 ±1.2

(range: 5-9; Table 1). Mean total band size in July did not differ signifi-

cantly from that in January (Kruskal-Wallis H = 2.98, p > 0.05), although

numbers of juveniles counted in July comprised a greater proportion of

animals (52.9%) than in January (24.7%). There were no significant dif-

ferences between the three meerkat bands in the size of any age-sex class,

nor were there significant differences in mean band size between years

(Kruskal-Wallis tests, p > 0.05 in all cases).

TABLE 1. Age-sex composition of three meerkat focal bands in the south-

western Kalahari, January and July 1985-1988

Key: R = Raiders, 0 = Outliers, W = Woodlanders. Ad = adult, Y = yearling, J = juvenile. Sex ratio expressed as proportion of males.


839

Most immigration took place at the yearling or two-year-old stages.

Among yearlings of known origin 64.3% of 14 males, but none of three

females were immigrants. In their second year, 75% of four males, and all

three females were immigrants, and during their third year all three male

and four females of known origin were immigrants.

Annual variation in population structure

When averaged across all bands, there was no significant annual variation

in population age structure (Table 2; Kruskal-Wallis ANOVA, p > 0.05).

Total band size tended to be higher in the first two years of the study,

varying from a high of 2.8 in 1985/'86 to a low of 5.3 =b 1.4 in

1986/' 87. There was little annual variation in the number of adults present 1.0 in 1986/'87 to 1.0 in 1987/'88) and most of the variation

was due to the number of yearlings, particularly females. Bands contained

a disproportionate amount of yearlings throughout the breeding season in

1985/'86, a year of pronounced drought (Kruskal-Wallis H = 7.05, p =

0.07).

TABLE 2. Annual variation in meerkat band composition in the southwestern

Kalahari, 19841'85 to 19871'88

Structure presented as the mean (SD) of the modal number of individuals of each age-sex class present within bands throughout the breeding season. Unsexed yearlings only included in yearling totals. Rep f = reproductive females.


840

Sex ratios

Sex was determined for kittens in 17 focal band litters at the time of first

emergence from the den and within a month of birth. The sex ratio of 0.40

did not differ significantly from equality (29 males, 43 females, and three

unknowns: Gad? = 2.72, 1 df, p > 0.05). Any mortality at the den prior to

the initial counts is unlikely to have affected the neonatal sex ratio since

the survival rates of males and females from first count to three months

were identical (Doolan & Macdonald, 1996b). Insufficient counts of sexed

juveniles were available from non-focal bands to assess juvenile sex ratio

for the overall population. However, records of an additional 95 males

and 113 females bom in captivity (International Zoo Yearbook 1967-1992) verified that the birth sex ratio of 0.46, although tending towards females,

was not significantly skewed (Gadj = 1.56, 1 df, p > 0.05). The overall sex-ratio of focal-band adults and yearlings combined was

not significantly different from unity, although it was biased towards males

(Table 1, January: Gadj = 1.98, 1 df, p > 0.05; July: Gadj = 1.65, 1 df,

p > 0.05). Nor was there a significant deviation from a 1 :1 sex ratio

within the juvenile, yearling or adult age classes, although the result for

yearlings in January bordered on significance (Gadj = 3.58, 1 df, p < 0.06).

There was also no significant sex bias in the operational sex ratio of 0.58

calculated from the modal numbers of adult males and reproductive females

present throughout the breeding season (Gadj = 1.51, 1 df, p > 0.05). A Kruskal-Wallis ANOVA of the number of males per female across all

band years showed no significant difference in sex ratio between years. At a population level, using data from both focal and non-focal bands,

there was no significant skew in the sex ratio for the total number of adults

(65 males: 60 females) or yearlings (26 males: 15 females; Gadj = 2.96,

1 df, p > 0.05, N = 25 band years) sexed over the study period. However,

there was a significant bias towards males (Gadj = 4.49, 1 df, p < 0.05,

N = 30 band years) in the overall operational ratio of adult males to

reproductive females (65 males: 43 females). The ratio of adult males to

reproductively active females tended to be more strongly biased towards

males in larger bands, but this was not statistically significant (rs = 0.35,

p = 0.06).


841

Band size and failures of reproductive suppression

A high proportion of adult females bred: 71.6% of 60 adult females were

classified as reproductive at some stage during the breeding season, and

plural breeding occurred in 40% of 30 band years (Table 3). There were

no significant differences between years in the proportion of reproductive

females (G = 1.12, 3 df, p > 0.05). The annual incidence of plural

breeding did not differ significantly between years (Table 3; G = 2.18,

3 df, p > 0.05).

Significantly more adults were present in plural breeding bands than

singular breeding bands (Mann-Whitney test, z = 2.41, Nl = 12, N2 = 18,

p < 0.02). On average, plural breeding bands contained 4.9 ±1.3 adults,

while singular breeding bands contained 1.1 adults (Table 4). There

were no differences between plural and singular breeding bands in total

band size or in the number of adult males present (Table 4), but plural

TABLE 3. Annual incidence of plural breeding in focal and non-focal

meerkat bands, monitored over 30 band-breeding years, 19841'85 to

19871'88

TABLE 4. Mean sizes (SD) of singular- and plural-breeding meerkat bands

in the southwestern Kalahari over 30 band-years, 19841'85 to 19871'88

Values calculated from modal numbers of animals present in each band throughout the

breeding season.


842

breeding bands contained significantly more adult females (x = 0.6) than singular breeding bands (x = 1 .5 + 0.5 ; Mann-Whitney test, z = 4.04,

Nl = 12, N2 = 18, p < 0.001). Plural breeding bands contained 2.1 ±0.3

reproductive females. Within bands, the number of reproductive females

was strongly correlated with the number of adult females (using all band

years as independent data points: rs = 0.73, N = 30, p < 0.001) but not

with the number of adult males (rs = 0.06, N = 30, p > 0.05).

Only 4 (16°l0) reproductive females in plural breeding bands were two-

year-old, whilst 17 (68%) were aged three years and above. Four individ-

uals were unclassified. The genetic relationship between the females was

unknown in all cases. In their first year in the Raiders and prior to the

establishment of a clear rank relationship, both females 23 and 24 were

simultaneously pregnant as two-year-olds. The other instances in which

young adults bred occurred in the presence of clearly dominant older an-

imals. Within the focal bands, one female (23) bred as a subordinate in

successive years.

Per capita reproductive success

Using each band year as an independent data point, the number of juveniles

produced per adult female was negatively correlated with the number of

adult females present in that band (rs = -0.56, N = 26, p < 0.003).

Similarly, per capita reproductive success for reproductive females declined

with the number of reproductive females present in that band (rs = -0.47, N = 26, p < 0.02). The number of adult males was also negatively related

to juvenile production per adult male (rs = -0.45, N = 26, p < 0.03).

Discussion

Among other gregarious carnivores such as dwarf mongooses Helogale

parvula (Rood, 1980, 1990; Rasa, 1987, 1989) and many canids (Moehl-

man, 1989), bands are basically extended families composed of a single

breeding pair and their philopatric offspring. By contrast, the data presented here demonstrate that a meerkat band is a multi-male, multi-female society, with yearlings and adults of both sexes dispersing and joining other bands.

Although the study was not sufficiently long-term to systematically deter-

mine relatedness, the degree of flux in band membership meant that many


843

individuals were non-kin, and the relative constancy in band size within

and between years masked considerable change in individual membership. The events surrounding forced emigration from bands (see also Doolan &

Macdonald, 1996b) are suggestive of the competition over breeding opportunities noted in other cooperative breeders (e.g. Mumme et al., 1983a, b;

Hannon et al., 1985; Curry, 1988). This is supported by several lines of

evidence. As for other gregarious species (e.g. Koenig, 1981; Mumme

et al., 1988; da Silva et al., 1994): per capita number of young produced to the end of the breeding season declined with group size for adult

males, adult females and reproductively active females. Some subordi-

nate females lost their litters to infanticide by dominant females (Doolan & Macdonald, 1996b) so the actual per capita value was further skewed.

Overall, the most prolonged and aggressive encounters within bands were

between older same-sex individuals, and coincided with mating periods

(see also Doolan & Macdonald, 1996b, in press). Although lower-ranking subordinates participated in these, they were not responsible for initiation

of struggles and aggressive targeting. Potential immigrants also encoun-

tered most resistance from residents of the same sex and dominant residents

were particularly aggressive towards adult intruders.

A previous short term study of meerkats by Roberts (1981) suggested that only a single female bred in each band, whereas Lynch (1980) indi-

cated that two females could be simultaneously pregnant. In the Kalahari,

plural breeding was widespread among meerkats, occurring in 40% of all

band years. Dominance rank in both meerkats and dwarf mongooses in-

creases with age (Rood, 1990; Creel et al., 1992, Doolan & Macdonald,

1996b). As with dwarf mongooses (Creel & Waser, 1991), plural breeding was most likely to occur in larger meerkat bands, and among older animals.

Banded mongooses Mungos mungo are apparently unusual among cooper-

atively breeding carnivores in that most females breed and only some are

suppressed (Rood, 1975; Sadie, 1983; Waser et al., in press).

Among dwarf mongooses subordinates are reproductively suppressed by both behavioral and endocrinal mechanisms (Creel et al., 1992; Keane

et al., 1994). Subordinate male dwarf mongooses are suppressed by ag-

gressive interruptions from dominant males during mating activity (Creel et al., 1992), or as a consequence of mating with infertile subordinate fe-

males (Rood, 1980). Younger subordinate females are less likely to become


844

pregnant because their hormonal levels are insufficient to trigger ovulation

whereas older, higher-ranking subordinates have higher levels of circulating hormones and are more likely to become pregnant and produce offspring. The fact that the only subordinate females to breed were at least three years old suggests that a similar endocrinal mechanism may contribute to reproductive suppression in female meerkats. Due to the sparsity of observations

of copulation during our study, we were unable to determine if subordinate

meerkat males were 'psychologically castrated' (Reyer, 1990) by ineffec-

tive endocrinal function, but Lynch's (1980) observations of sperm in the

epididymes of yearling males suggests that behavioural mechanisms may be more important.

As with wolves Canis lupus (see Derix et al., 1993), dominant female

meerkats physically interfere with the reproductive behaviour of subordi-

nates ; dominants are particularly aggressive towards oestrous yearlings and

other adult females during mating periods (Doolan & Macdonald, 1996b).

Four heavily pregnant meerkats were observed being attacked by band

members led by the dominant female, and plural breeding subordinates

frequently suffered perinatal losses of their litters, apparently to infanticide

by dominant females (Doolan & Macdonald, in press). Dominants also ap-

peared to prevent subordinates from breeding within bands by forcing them

to emigrate to escape aggression (Doolan & Macdonald, 1996b). Hence

reproductive suppression among females can be enforced rather than solely

being endocrinal in origin.

However, older subordinate meerkat females also used emigration to

acquire breeding rank in other bands (Doolan & Macdonald, 1996b): older

females immigrated into bands at a higher rate than yearlings, and two

of three known breeding female vacancies were filled by immigrants. In

effect, this weakens the 'power of veto' exerted by dominant females (Noe,

1990) so that subordinates have greater 'leverage' (Vehrencamp, 1983;

Creel & Waser, 1991) to 'negotiate' with dominants over reproductive

opportunities (Dunbar, 1988). The positive relationship between number

of adult female meerkats and number of reproductive females may reflect

the increasing difficulty that dominant animals have in monitoring mating

activity in larger bands. Dominant male dwarf mongooses also monopolise

mating less efficiently when packs are scattered or when some individuals

seek seclusion (Rasa, 1985; Creel et al., 1992).


845

Carnivores are renowned for the flexibility of their social organisation

(Macdonald, 1983, 1992). Research on dwarf mongooses has uncovered

enormous complexity in the behavioural tactics adopted by individuals

(Rood, 1980, 1990; Rasa, 1989; Creel et al., 1992; Creel & Waser, 1994, in press). Creel & Waser's (1991) analysis of the inclusive fitness pay- offs for philopatric and dispersing female dwarf mongooses has shown

that the degree to which groups are despotic or egalitarian varies with

demographic structure. Plural breeding is most prevalent in packs which

contain older, high-ranking subordinates whereas reproductive suppression is more evident in packs which contain only young, low-ranking subordi-

nates. Kalahari meerkats employ a similarly diverse range of reproductive

strategies (see also Doolan & Macdonald, 1996b, in press). Males and

females disperse frequently, with male coalitions invading and taking over

bands. Bands exhibiting failures of reproductive suppression live along- side singular-breeding bands containing reproductively suppressed adult

females. The variability evident within meerkat society arises because in-

dividuals respond to the opportunities afforded by their age, status and the

structure of their bands.

References

Acocks, J.P.H. (1988). Veld types of South Africa. - Memoirs Bot. Survey S. Africa 57, p. 1-146.

Altmann, S.A. & Altmann, J. (1979). Demographic constraints on behavior and social organization. - In: Primate ecology and human origins: Ecological influences on social organization (E. Bernstein & F. Smith, eds). Garland, New York, p. 47-63.

Bekoff, M., Daniels, T.J. & Gittleman, J.L. (1984). Life history patterns and the comparative social ecology of carnivores. - Ann. Rev. Ecol. Syst. 15, p. 191-232.

Brown, J.L. (1987). Helping and communal breeding in birds. - Princeton University Press, Princeton.

Creel, S.R., & Creel, N.M. (1991). Energetics, reproductive suppression and obligate communal breeding in carnivores. - Behav. Ecol. Sociobiol. 28, p. 263-270.

-, - -, Wildt, D.E. & Monfort, S.L. (1992). Behavioral and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. - Anim. Behav. 43, p. 231- 245.

- - & Macdonald, D.W. (1995). Sociality, group size and reproductive suppression among carnivores. - Adv. Study Behav. 24, p. 203-257.

- - & Waser, P.M. (1991). Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation? - Behav. Ecol. 2, p. 7-15.

- - & - - (1994). Inclusive fitness and reproductive strategies in dwarf mongooses. - Behav. Ecol. 5, p. 339-348.


846

- - & - - (in press). Variation in reproductive suppression in dwarf mongooses: in-

terplay between evolution and mechanisms. - In: Cooperative breeding in mammals

(J. French & N. Solomon, eds). Princeton University Press, Princeton, New Jersey. Curry, R.L. (1988). Group structure, within-group conflict, and reproductive tactics in

cooperatively-breeding Galapagos mockingbirds, Nesomimus parvulus. - Anim. Be- hav. 36, p. 1708-1728.

- - & Grant, P.R. (1989). Demography of the cooperatively breeding Galapagos mock-

ingbird, Nesomimus parvulus, in a climatically variable environment. - J. Anim. Ecol. 58, p. 441-464.

Derix, R., van Hooff, J., de Vries, H. & Wensing, J. (1993). Male and female mating competition in wolves: female suppression vs male intervention. - Behaviour 127,

p. 141-174. Doolan, S.P. (1994). The behavioural ecology of the suricate, Suricata suricatta, in the

southwestern Kalahari. - D. Phil. thesis, University of Oxford. - - & Macdonald, D.W. (1996a). Diet and foraging behaviour of group-living meerkats,

Suricata suricatta, in the southern Kalahari. - J. Zool. (Lond.) 239, p. 697-716. - - & - - (1996b). Dispersal and extra-territorial prospecting by slender-tailed

meerkats (Suricata suricatta) in the southwestern Kalahari. - J. Zool. (Lond.) 240,

p. 59-73. - - & - - (in press). Breeding and juvenile survival among slender-tailed meerkats

(Suricata suricatta) in the southwestern Kalahari: ecological and social influences. J. Zool. (Lond.)

Dunbar, R.I.M. (1979). Population demography, social organization and mating strategies. - In: Primate ecology and human evolution (I.S. Bernstein & E.O. Smith, eds). Garland, New York, p. 65-88.

- - (1988). Primate social systems. - Croom Helm, London. - - (1989). Social systems as strategy sets: the costs and benefits of sociality. - In:

Comparative socioecology: The behavioural ecology of humans and other mammals

(V. Standen & R.A. Foley, eds). Blackwell Scientific Publications, Oxford, p. 131-149.

Emlen, S.T. (1991). Evolution of cooperative breeding in birds and mammals. - In: Be- havioural ecology: an evolutionary approach (J.R. Krebs & N.B. Davies, eds). Black- well Scientific Publications, Oxford, p. 301-337.

- - & Wrege, P.H. (1994). Gender, status and family fortunes in the white-fronted bee- eater. - Nature 367, p. 129-132.

Ewer, R.F. (1963). The behaviour of the meerkat, Suricata suricatta (Schreber). -

Z. Tierpsychol. 20, p. 570-607. Gittleman, J.L. (1985). Functions of communal care in mammals. - In: Evolution: es-

says in honour of John Maynard Smith (P.H. Harvey & M. Slatkin, eds). Cambridge University Press, Cambridge, p. 187-205.

- - (1989). Carnivore group living comparative trends. - In: Carnivore behaviour, ecology, and evolution (J.L. Gittleman, ed.). Chapman & Hall, London, p. 183-207.

Hannon, S.J., Mumme, R.L., Koenig, W.D. & Pitelka, F.A. (1985). Replacement of breeders and within-group conflict in the cooperatively breeding acorn woodpecker. - Behav. Ecol. Sociobiol. 17, p. 303-312.

Keane, B., Waser, P.M., Creel, S.R., Creel, N.M., Elliott, L.F. & Minchella, D.J. (1994). Subordinate reproduction in dwarf mongooses. - Anim. Behav. 47, p. 65-75.


847

Keller, L. & Reeve, H.K. (1994). Partitioning of reproduction in animal societies. - Trends Ecol. Evol. 9, p. 98-102.

Koenig, W.D. (1981). Reproductive success, group size, and the evolution of cooperative breeding in the acorn woodpecker. - Am. Nat. 117, p. 421-443.

- -, Pitelka, F.A., Carmen, W.J., Mumme, R.L. & Stanback, M.T. (1992). The evolution of delayed dispersal in cooperative breeders. - Quart. Rev. Biol. 67, p. 111-150.

Leistner, O.A. (1967). The plant ecology of the southern Kalahari. - Memoirs Bot. Survey S. Africa 38, p. 1-172.

Ligon, J.D., Ligon, S.H. & Ford, H.A. (1991). An experimental study of the basis of male philopatry in the cooperatively breeding superb fairy wren Malurus cyaneus. -

Ethology 87, p. 134-148.

Lynch, C.D. (1980). Ecology of the suricate, Suricata suricatta, and the yellow mongoose, Cynictis penicillata, with special reference to their reproduction. - Memoirs Nas. Mus. Bloemfontein 14, p. 1-145.

Macdonald, D.W. (1983). The ecology of carnivore social behaviour. - Nature 301, p. 379- 384.

- - (1992). The velvet claw: a natural history of the carnivores. - BBC Publications, London.

- - & Carr, G.M. (1989). Food security and the rewards of tolerance. - In: Comparative socioecology: The behavioural ecology of humans and other mammals (V. Standen & R.A. Foley, eds). Blackwell Scientific Publications, Oxford, p. 75-99.

- - & Moehlman, P.D. (1983). Co-operation, altruism and restraint in the reproduction of carnivores. - In: Perspectives in ethology 5 (P.P.G. Bateson & P.H. Klopfer, eds). Plenum Press, New York, p. 433-466.

Malcolm, J.R. & Marten, K. (1982). Natural selection and the communal rearing of pups in African wild dogs (Lycaon pictus). - Behav. Ecol. Sociobiol. 10, p. 1-13.

Moehlman, P.D. (1989). Intraspecific variation in canid social systems. - In: Carnivore behavior, ecology, and evolution (J.L. Gittleman, ed.). Chapman & Hall, London, p. 143-164.

Mumme, R.L., Koenig, W.D. & Pitelka, F.A. (1983a). Mate guarding in the acorn wood-

pecker : within-group reproductive competition in a cooperative breeder. - Anim. Behav. 31, p. 1094-1106.

- , - & - - (1983b). Reproductive competition in the communal acorn wood-

pecker : sisters destroy each other's eggs. - Nature 306, p. 583-584. - -,- - & - - (1988). Costs and benefits of joint nesting in the acorn woodpecker.

- Am. Nat. 131, p. 654-677. Noe, R. (1990). A Veto game played by baboons: A challenge to the use of the Prisoner's

Dilemma as a paradigm for reciprocity and cooperation. - Anim. Behav. 39, p. 78-90. Packer, C. (1986). The ecology of sociality in felids. - In: Ecological aspects of social

evolution: birds and mammals (D.I. Rubenstein & R.W. Wrangham, eds). Princeton

University Press, Princeton New Jersey. Rasa, O.A.E. (1985). Mongoose watch. - John Murray, London. - - (1987). The dwarf mongoose: a study of behaviour and social structure in a small,

social carnivore. - Adv. Study Anim. Behav. 17, p. 121-163.


848

- - (1989). Helping in dwarf mongoose societies: An alternative reproductive strategy. - In : The sociobiology of sexual and reproductive strategies (O.A.E. Rasa & C. Vogel, eds). Croom Helm, London, p. 61-73.

Reyer, H.-U. (1990). Pied kingfishers: ecological causes and reproductive consequences of cooperative breeding. - In: Cooperative breeding in birds (P.B. Stacey & W.D. Koenig, eds). Cambridge University Press, p. 527-558.

Roberts, K.S. (1981). The foraging behaviour and strategies of the suricate Suricata suricatta (Erxleben). - MSc Dissertation, University of Pretoria.

Robinson, J.G. (1988a). Demography and group structure in wedge-capped capuchin mon-

keys, Cebus olivaceus. - Behaviour 104, p. 202-232. - - (1988b). Group size in wedge-capped capuchin monkeys Cebus olivaceus and the

reproductive success of males and females. - Behav. Ecol. Sociobiol. 23, p. 187-197. Rood, J.P. (1975). Population dynamics and food habits of the banded mongoose. - E. Afr.

Wildl. J. 13, p. 89-111. - - (1980). Mating relationships and breeding suppression in the dwarf mongoose. -

Anim. Behav. 28, p. 143-150. - - (1986). Ecology and social evolution in the mongooses. - In: Ecological aspects

of social evolution: birds and mammals (D.I. Rubenstein & R.W. Wrangham, eds). Princeton University Press, Princeton, New Jersey, p. 131-152.

- - (1990). Group size, survival, reproduction, and routes to breeding in dwarf mon-

gooses. - Anim. Behav. 39, p. 566-572. Russell, E.M. & Rowley, I. (1993). Philopatry or dispersal: competition for territory vacan-

cies in the splendid fairy wren, Malurus splendens. - Anim. Behav. 45, p. 519-539. Sadie, D. (1983). The foraging behaviour and metabolic rate of the banded mongoose

Mungos mungo (Gmelin). - MSc thesis, University of Pretoria, Pretoria. da Silva, J., Macdonald, D.W. & Evans, P.G.H. (1994). Net costs of group living in a

solitary forager, the Eurasian badger. - Behav. Ecol. 5, p. 151-158. Sokal, R.R. & Rohlf, F.J. (1981). Biometrics. - Freeman, San Francisco.

Stacey, P.B. & Ligon, J.D. (1991). The benefits-of-philopatry hypothesis for the evolution of cooperative breeding: variance in territory quality and group size effects. - Am. Nat. 137, p. 831-846.

Vehrencamp, S.L. (1983). A model for the evolution of despotic versus egalitarian societies. - Anim. Behav. 31, p. 667-682.

Vick, L.G. & Pereira, M.E. (1989). Episodic targeting aggression and the histories of Lemur social groups. - Behav. Ecol. Sociobiol. 25, p. 3-12.

Waser, P.M., Elliott, L.F., Creel, N.M. & Creel, S.R. (in press). Habitat variation and

mongoose demography. - In: Serengeti II: Research, management and conservation of an ecosystem (A.R.E. Sinclair & P. Arcese, eds). University of Chicago Press, Chicago.


band structure and failures of reproductive …...maurice calvert-evers and john elford of nissan...

Documents