Robbing rivals: interference foraging competition reflects female reproductive competition in a cooperative mammal

Animal Behaviour 112 (2016) 229e236

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Robbing rivals: interference foraging competition reflects female reproductive competition in a cooperative mammal Lynda L. Sharpe, Janneke Rubow, Michael I. Cherry* University of Stellenbosch, Stellenbosch, South Africa

a r t i c l e i n f o Article history: Received 31 July 2015 Initial acceptance 16 September 2015 Final acceptance 5 November 2015 Available online MS. number: 15-00658R Keywords: dwarf mongoose Helogale parvula interference foraging competition intrasexual competition kleptoparasitism prey theft social selection

Intense intrasexual competition for breeding opportunities is a characteristic of cooperatively breeding species with high reproductive skew. In such ‘singular’ cooperative breeders, females suffer greater variability in direct reproductive success than do males, and this in turn leads to greater intrasexual competition in females. Under such circumstances, selection should favour traits that enhance female competitive ability, such as size, fighting skill or aggression. However, despite burgeoning interest in female intrasexual competition, there is limited evidence that female cooperative breeders exhibit more pronounced competitive traits than do males. We examined whether intrasexual competition has influenced the expression of a competitive behavioural trait (i.e. prey theft) in a ‘singular’, cooperatively breeding mammal, the dwarf mongoose, Helogale parvula. We used both observational and experimental data to assess whether wild dwarf mongooses exploit interference foraging competition to persecute their reproductive rivals, and whether the sexes differ with regard to this behaviour. We found that nonalpha female mongooses preferentially stole from other females rather than males, and that, under natural foraging conditions, they were more likely to steal prey from their closest rival (i.e. the female immediately below themselves in the dominance hierarchy) than from easier targets much lower in rank. In contrast, male dwarf mongooses (and alpha females) did not exhibit any sex bias, stealing prey indiscriminately from all lower ranking group members. We conclude that the acute intrasexual rivalry suffered by female dwarf mongooses has led to the differential development of this competitive behavioural trait. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Intrasexual competition in male vertebrates has attracted much scientific study, and we now understand the critical role of sexual selection in the evolution of male ornamentation, weaponry and behaviour (Andersson, 1994). However, intrasexual competition for breeding opportunities is also an important selective force in females (Clutton-Brock, et al., 2006; Clutton-Brock, 2009a) particularly where females compete for male parental care (Andersson, 2004; Emlen & Oring, 1977) or vary in their ability to rear young due to the scarcity of a particular resource (Heinsohn, Legge, & Endler, 2005; Hofer & East, 2003). Intense female reproductive competition is also a characteristic of cooperatively breeding species, especially ‘singular’ cooperative breeding, in which one female monopolizes reproduction within the group and many females are unable to breed at all (Clutton-Brock, 2009b). Within cooperative breeders the reproductive success of females is often more variable than that of males (Hauber & Lacey, * Correspondence: M. I. Cherry, Department of Botany and Zoology, University of Stellenbosch, Private Bag XI, Matieland, 7602, South Africa. E-mail address: [email protected] (M. I. Cherry).

2005) due to longer tenure in female breeders and more complete reproductive suppression of female subordinates (Young & Bennett, 2013). This generates greater intrasexual competition in females than males, and will favour selection in females for traits that enhance competitive ability, such as size, fighting skill and aggression (Clutton-Brock, et al., 2006; Hodge, Manica, Flower, & Clutton-Brock, 2008; Holekamp & Smale, 2000; Ostner, Heislermann, & Kappeler, 2003; Reeve & Sherman, 1991). As a result, female cooperative breeders could be expected to exhibit more pronounced development of these traditionally ‘male’ traits than do conspecific males. Yet despite burgeoning scientific interest in the causes and evolutionary consequences of female intrasexual competition (Clutton-Brock & Huchard, 2013a,b; Rubenstein & Lovette, 2009; Stockley & Bro-Jorgensen, 2011; Young & Bennett, 2013), there is little empirical evidence that females in cooperatively breeding species exhibit differential exaggeration of competitive traits relative to male conspecifics (Stockley & BroJorgensen, 2011; Young & Bennett, 2013). To date the strongest evidence is derived from research on cooperatively breeding meerkats, Suricata suricatta. Female

http://dx.doi.org/10.1016/j.anbehav.2015.12.009 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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meerkats exhibit higher rates of intrasexual aggression than males (Clutton-Brock, et al., 2006; Sharpe, 2005) and, once they acquire a breeding position, undergo a secondary growth spurt in body length that is not seen in males (Russell, Carlson, McIlrath, Jordan, & Clutton-Brock, 2004), presumably to assist in the suppression of reproductive rivals (Clutton-Brock, et al., 2006). In many cooperative species, females are more efficient than males at suppressing reproduction in same-sex subordinates (e.g. dwarf mongooses, Keane et al. 1994; naked mole-rats, Heterocephalus glaber, Reeve, Westnest, Noon, Sherman, & Aquado, 1990; Damarland mole-rats, Cryptomys damarensis, Burland, Bennett, Jarvis, & Faulkes, 2002; common marmosets, Callithrix jacchus, Abbott, 1984) and often employ more elaborate or extreme mechanisms to achieve this (Hauber & Lacey, 2005), such as eviction or infanticide (e.g. Cant, Hodge, Bell, Gilchrist, & Nichols, 2010; Clutton-Brock, et al., 1998). In this study, we examined whether intrasexual competition has influenced the expression of a competitive behavioural trait in a cooperatively breeding mammal, the dwarf mongoose. We assessed whether patterns of interference foraging competition support the tenet that mongooses use foraging competition to repress reproductive rivals, and whether the sexes differ in this behaviour. Interference foraging competition (also called ‘contest’ or ‘direct’ competition) occurs when one individual actively excludes others from a food source (Isbell, 1991). In a number of social primate and carnivore species, dominant individuals use interference competition to limit subordinates' access to food, thereby lowering subordinate reproductive success (Sterck, Watts, & van Schaik, 1997; Stockley & Bro-Jorgensen, 2011). For example, in vervet monkeys, Chlorocebus pygerythrus, birth rate is correlated with female rank only when the monkeys' preferred food species are clumped in distribution during the breeding period, thereby allowing high-ranking females to exclude subordinates (Whitten, 1983). Similarly, the monopolization of carcasses by high-ranking female spotted hyaenas, Crocuta crocuta, results in a correlation between female rank and fertility that grows stronger during periods of prey scarcity (Holekamp, Smale, & Szykman, 1996). However, little is known of the impact of interference foraging competition in cooperative breeders. Among the cooperative mongoose species, interference competition, in the form of prey theft, is common (Flower, 2007; de Luca & Ginsberg, 2001; Rood, 1975; Sharpe, Hill, & Cherry, 2013), but its potential role in reproductive competition has received little attention. This is primarily because the social mongooses prey on cryptic, widely dispersed invertebrates that are difficult for one individual to monopolize (Flower, 2007). Nevertheless, it has been demonstrated in meerkats that the dominant female steals more readily from female subordinates than from male subordinates, and from older females (which are more likely to reproduce; Clutton-Brock, et al., 2001) than young females, suggesting that prey theft could play a role in reproductive suppression in this species (Flower, 2007). Dwarf mongooses are small (280 g), diurnal carnivores that live in territorial groups of 3e30 individuals in the wooded savannahs of sub-Saharan Africa. Groups normally comprise an alpha pair (which largely monopolizes breeding; Keane, et al., 1994), their adult offspring, the alpha female's sisters and one to three immigrant males. Group members show a strong, linear dominance hierarchy (Sharpe, et al., 2013) and no sexual size dimorphism (Sharpe, Jooste, & Cherry, 2012). Females normally remain in their natal group for life, queuing to inherit the alpha position (Rood, 1990). If the queue is long (Keane, Creel, & Waser, 1996) or they lose rank to a younger sibling (L. L. Sharpe, personal observation), females will also disperse (occasionally in twos), but they cannot join existing groups that contain more than one female (Rood, 1986) and must establish new groups. Thus reproductive competition in females remains exclusively intragroup. In contrast, males

normally disperse at 2e3 years of age (usually in coalitions), joining other established groups (either as subordinates or by ousting the resident males) or founding new groups (Rood, 1990). They often change group more than once and thus compete with unrelated males as well as siblings. It has been estimated that female dwarf mongooses exhibit greater variation in direct reproductive success than males (Hauber & Lacey, 2005). This is because alpha females enjoy life-long tenure (whereas alpha males are frequently ousted by immigrants; Rood, 1986): females are not only likely to attain greater fitness benefits from alpha status, but nonalpha females obtain fewer opportunities to secure an alpha position. Female dwarf mongooses are also less able than males to reproduce successfully prior to obtaining an alpha position (mothering only 14% of offspring reared by their group, compared with 24% fathered by nonalpha males; Keane, et al., 1994). We used both observational and experimental data to determine whether wild dwarf mongooses use interference competition to deprive their reproductive rivals of food. The theft of prey from sexual rivals could benefit the thief in two ways: first by intimidating a competitor and thus reinforcing the thief's position in the dominance hierarchy and second by depriving the rival of resources during periods of food stress so that its competitive ability (relative to the thief) is reduced. If reproductive competition is a motivating factor for interference foraging competition in dwarf mongooses, we predict that (1) individuals will steal prey primarily from samesex subordinates (because reproductive competition occurs within a sex) and (2) individuals will preferentially steal prey from samesex subordinates that are immediately below themselves in the dominance hierarchy (because these individuals pose the greatest threat). We also predict that these preferences will be more pronounced in female dwarf mongooses because this sex appears to show greater variation in direct inclusive fitness (Hauber & Lacey, 2005) and hence suffers more intense intrasexual competition. Additionally, female dwarf mongooses, unlike males, compete with the same individuals throughout their lives, until they either gain alpha status or die, which is likely to promote intense rivalry. METHODS Study Population We undertook the research between June 2006 and November 2014 at Phuza Moya Private Game Reserve, northeastern South Africa (24160 1000 S, 30470 4600 E). Climate and vegetation are described in the electronic supplement of Sharpe, Joustra, and Cherry (2010). We collected the data from eight wild dwarf mongoose groups (mean group size 13.5) that were habituated to an observer walking within 2e3 m. All group members were individually ID-marked using Nutrisse blonde hair dye (Garnier, London), which we applied with a long-handled paintbrush while the mongooses were basking in the early morning sunshine. We visited groups at least three times per week throughout the study period to monitor changes in group composition and document agonistic interactions (i.e. overt aggression, submissive behaviour or displacements at a resource), and the dominance hierarchy for all group members was known at all times. Ethical Note All methods conform to the laws of South Africa and were approved by Stellenbosch University's research committee (application number: 2009 B001002). No mongoose in this study population has ever been captured or directly handled and we have

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never observed an adverse reaction to the hair dye used for ID marking. The mongooses do not ingest the dye via grooming, as they find it distasteful. To minimize any impact of the manipulation experiment, we kept sample sizes small, and we observed no apparent change in the social interactions of participants (i.e. victims and thieves) after the experiments. Natural Prey Theft Dwarf mongooses forage by day as a cohesive group, with each mongoose independently scratching through the soil for arthropods and the occasional small vertebrate (Rasa, 1973). During the cool winter dry season, when invertebrates are scarce, individuals often steal prey from lower ranking group members (Sharpe, et al., 2013). It is unusual for a mongoose to steal an item directly from the finder (because invertebrate prey are small enough to be eaten quickly) but the mongooses frequently commandeer the foraging hole of an individual excavating fossorial prey. The thief normally approaches its victim hip-first, while producing deep growls, and the victim rarely offers any resistance, rapidly abandoning its excavation while making high-pitched submissive calls (Sharpe, et al., 2013). We accompanied groups on foot during their morning foraging session and used ad libitum sampling (Altmann, 1974) to document thefts of foraging excavations. We recorded the identity of both thief and victim, documenting 179 thefts, perpetrated by 71 adult mongooses from eight groups. Adult mongooses did not steal from youngsters less than 4 months old, and in only four cases did we observe a mongoose steal prey from a higher ranking group member (these thefts were excluded from the analysis). Although thefts were relatively common during the winter, it was often impossible to identify both participants (due to the speed of the interaction and the vegetation cover), so we cannot provide reliable data on rates of prey theft. Body Weight To assess whether prey theft had an effect on an individual's body condition, we documented individual weight changes over the experimental period (JuneeAugust 2014). We weighed the mongooses first thing in the morning (before they began foraging) by coaxing each individual to stand on an electronic balance (Sartorius B13; capacity 3000 g, accuracy 1 g) using a few crumbs (<0.5 g) of boiled egg. We collected weight measurements for 4 days at the start of the experimental period and again, 10 weeks later, at the end of the period. Measurements (at start and finish) were averaged for each individual, and were used to calculate weight change (g) for 45 adult mongooses (21 males and 24 females) from four groups. Manipulation Experiments We undertook experiments in four groups (mean group size 13) in JuneeAugust 2014. During the 3 months prior to the experiments we documented natural agonistic interactions (i.e. displacements, aggression or submission) using ad libitum sampling (Altmann, 1974). We recorded the identity and role of participants in 1017 dyadic interactions (range 116e428 per group) and used the I & SI method (de Vries, 1998) to calculate the ordinal dominance rank of all individuals within each group. To achieve this, we compiled a ‘win/lose’ matrix for each group which listed an individual's ‘wins’ (or assertions of dominance) beside its row name and its ‘losses’ (submissions) under its column name. An individual was considered dominant to another group member if its ‘wins’ outnumbered its ‘losses’ in interactions between the two. We then rearranged the

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order of individuals within the matrix to reflect these dyadic relationships. Pairs with an unknown relationship (no encounters observed) or tied relationship (‘wins’ equalled ‘losses’) were ordered based on the relative number of group members each partner dominated (except where this generated inconsistencies; de Vries, 1998). The linearity of the resultant hierarchies did not show any reversals (i.e. A > B and B > C but C > A). We undertook two different manipulation experiments: the ‘sex experiment’, to test whether test subjects were more likely to steal from same- or opposite-sex subordinates, and the ‘rank experiment’, to test whether they were more likely to steal from their closest rival (i.e. the same-sex subordinate that ranked immediately below them in the hierarchy) or from a more lowly ranked, samesex subordinate. For the sex experiment, we tested the preferences of 11 adult (>12 months) nonalpha males and 11 adult nonalpha females. For the rank experiment, we tested 10 nonalpha adults of each sex. Whenever possible we used different test subjects for the sex and rank experiments; however, by necessity, some individuals acted as a test subject in both. When conducting an experiment, we ascertained the preferences of a test subject by subjecting it to two trials (with a different potential victim at each trial). The trials were conducted sequentially but ordered randomly. At a trial, we presented a small plastic dish (9  9 cm and 3 cm deep), that was half-filled with sand and contained 15 buried mealworms, Tenebrio molitor, to the intended victim (a group member of lower rank than the test subject). Once the intended victim began excavating mealworms, we lured the test subject (the intended thief) to within 8 cm of the dish using crumbs of boiled egg or cooked chicken. Other group members were kept away from the presentation area by tossing the same food items. We videoed the interaction using a Sony Handycam DCR-SX60E video recorder, beginning when the intended victim started excavating mealworms and concluding when all mealworms were eaten or the remaining mongoose lost interest. In total, we undertook 84 trials (44 for the sex experiment and 40 for the rank experiment). Prior to the experiments, all participants (victims and thieves) were individually trained to associate the dish with food and to access buried mealworms. Experiments were undertaken before the group began to forage in the morning to ensure all participants were hungry. Whenever possible we used individual victims in only one trial, but if an individual victim had to be used more than once (due to a limited number of group members) we ensured that it played a different role in each trial (same-sex victim, opposite-sex victim, closest rival, etc.). Video Analysis One observer reviewed all the videos and classified each trial as ‘theft’ (the test subject pushed the victim off the dish and ate the remaining worms; 40.7% of trials), ‘share’ (both individuals ate simultaneously from the dish or the victim obtained some worms after being pushed off; 34.5% of trials) or ‘no-theft’ (the test subject was either unable (37.9%), or did not try (62.1%), to obtain any worms; 24.8% of trials). To ensure that there was no observer bias, a second observer (blind to the identity and sex of the participants) reclassified 26% of the video data (22 trials). The results obtained by the two observers were the same for 21 of the 22 trials, resulting in a kappa statistic of 0.933 (Kaufman & Rosenthal, 2009). For trials in which the test subject stole the prey item (N ¼ 60), we analysed the videos using freeze-frame mode in K-Multimedia Player (R2) to determine how long it took the thief to oust the victim. To quantify duration we counted the frames (25/s), beginning when the thief first touched the dish and ending when the victim was no longer touching the dish or interacting with the thief.

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In cases of prolonged altercation, the interaction was considered finished if the victim left the dish for more than 1 min.

60 50

For each natural theft, we quantified the number of same- and opposite-sex potential victims present in the group (i.e. group members >4 months old that were of lower rank than the thief at the time of the theft) and the sex of the victim. We then averaged these data for each individual thief (mean observed thefts per thief ¼ 2.49 ± 0.29) and used individual thieves as sampling points to avoid pseudoreplication. We summed the individual values for all thieves within a particular sex/status category (alpha females N ¼ 10, nonalpha females N ¼ 27, alpha males N ¼ 8 and nonalpha males N ¼ 27), and these totals (rounded into integers) were then used in a contingency table to test whether the proportion of actual victims that were the same sex differed significantly from the proportion of potential victims that were the same sex. A similar procedure was used when testing whether thieves preferentially targeted their closest rival (i.e. the same-sex subordinate immediately below themselves in the hierarchy). In this case, a contingency table was used to test whether the proportion of same-sex victims that were the thief's closest rival (rather than lower-ranked animals) differed from the proportion of potential victims (same-sex subordinates) that were closest rivals. These chi-square tests were performed using SigmaStat Version II (IBM, Armonk, NY, U.S.A.). To assess whether the degree of weight loss over the winter was related to dominance rank, we tested whether an individual's weight change over the 10-week experimental period was correlated with the number of potential victims available to that individual (i.e. group members >4 months old that were lower ranking than the individual). We used a general linear model (GLM; performed in Statistica 12.0) to test whether number of potential victims (continuous predictor variable) in conjunction with group, age (months) and sex (categorical predictor variables) affected weight change. For the analysis of the experimental data, test subjects were given a score based on the outcome of each experimental trial: 2 for theft, 1 for sharing and 0 for no theft. We then used nonparametric matched-pair tests, performed in SigmaStat Version II, to assess whether individual test subjects were more likely to steal from a specific sex (same versus opposite, N ¼ 11 males, N ¼ 11 females) or rank (adjacent versus lower ranking, N ¼ 10 males, N ¼ 10 females). To test for a difference in the speed with which male and female thieves stole, we averaged the speed of thefts undertaken by an individual test subject (N ¼ 11 males, N ¼ 11 females) and then used a series of ManneWhitney U tests (performed in Statistica 12.0) to compare the sexes and test whether the speed of theft depended on the sex of the victim. All P values are two tailed and means are shown ± SE. RESULTS Natural Thefts Based on the number of natural thefts observed, alpha female mongooses were twice as likely as alpha males to commandeer the foraging holes of their subordinates, and four times as likely as the average nonalpha adult (chi-square test: c21 ¼ 55.67, P < 0.001; Fig. 1). Females (N ¼ 37) stole more frequently from same-sex victims, targeting female subordinates 54% more often than would be expected by chance (c21 ¼ 10.57, P ¼ 0.001). From among their samesex subordinates, female thieves chose to steal significantly more often than expected from their closest rival (i.e. the female

Number of thefts

Statistical Analysis

40 30 20 10 0

Alpha female

Alpha male

Beta female

Beta male

Mean < beta female

Mean < beta male

Figure 1. The number of incidents of theft observed when mongooses were foraging. ‘Mean < beta’ refers to the average for an adult group member of lower rank than the beta.

immediately below them in the dominance hierarchy; c21 ¼ 5.51, P ¼ 0.034). However, these findings appear to be the result of the behaviour of nonalpha females only (N ¼ 27; victim's sex: c21 ¼ 9.45, P ¼ 0.002; immediate subordinate: c21 ¼ 11.72, P < 0.001; Fig. 2). Alpha females (N ¼ 10) did not discriminate between victims on the basis of sex (c21 ¼ 0.65, P ¼ 0.42; Fig. 2a) although they did show a statistically nonsignificant tendency to steal more often than expected from the group's beta female (c21 ¼ 2.84, P ¼ 0.092; Fig. 2b). Male thieves (N ¼ 35) did not preferentially target victims of either sex (c21 ¼ 0.41, P ¼ 0.521), although they showed a nonsignificant tendency to steal from their immediate same-sex subordinate (c21 ¼ 2.96, P ¼ 0.081). Both alpha males (N ¼ 8) and nonalpha males (N ¼ 27) behaved in a similar manner (alpha: victims' sex: c21 ¼ 0.27, P ¼ 0.606; immediate subordinate: c21 ¼ 0.02, P ¼ 0.884; nonalpha: sex: c21 ¼ 1.32, P ¼ 0.25; immediate subordinate: c21 ¼ 2.1, P ¼ 0.148; Fig. 2). Manipulation Experiments During the experiments, nonalpha dwarf mongooses were more likely to steal from same-sex subordinates than opposite-sex subordinates (Wilcoxon signed-rank test: W ¼ 63.0, N ¼ 22, P ¼ 0.049; Fig. 3). However, this result was primarily due to the behaviour of females. Females stole significantly more often from females than from males (Wilcoxon signed-rank test: W ¼ 21.0, N ¼ 11, P ¼ 0.031), whereas males showed no apparent preference (W ¼ 11.0, N ¼ 11, P ¼ 0.461). When stealing from same-sex individuals, test subjects showed no apparent preference for victims based on their relative rank (Wilcoxon signed-rank test: W ¼ 18, N ¼ 20, P ¼ 0.594). Both male and female test subjects stole no more often from same-sex victims immediately below them in the hierarchy than from subordinates far below them (Wilcoxon signed-rank test: males: W ¼ 6.0, N ¼ 10, P ¼ 0.563; females: W ¼ 6.0, N ¼ 10, P ¼ 0.25). The speed with which a thief ousted its victim during an experimental trial was dependent on the sex of the thief. Female test subjects stole significantly faster than male test subjects (ManneWhitney U test: U ¼ 19.00, N1 ¼ 10, N2 ¼ 9, P ¼ 0.037; Fig. 4). However, speed of theft was unrelated to the sex of the victim (U ¼ 78.50, N1 ¼ 13, N2 ¼ 14, P ¼ 0.56). Thus neither female (U ¼ 16.00, N1 ¼ 9, N2 ¼ 4, P ¼ 0.817) nor male (U ¼ 17.00, N1 ¼ 9,

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Proportion of thefts directed at same-sex subordinates

0.9 0.8 (a)

*

0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

Alpha female Alpha male

Nonalpha female

Nonalpha male

Proportion of thefts directed at immediate same-sex subordinate

0.5 (b) *

0.4 0.3 0.2 0.1 0

Alpha female Alpha male N = 10 N=8

Nonalpha female N = 27

Nonalpha male N = 27

Figure 2. (a) The mean proportion of natural prey thefts directed towards same-sex victims (grey bars) and the proportion expected by chance (white bars) based on the number of lower ranking males and females in the group. (b) The mean proportion of natural prey thefts directed at the thief's immediate, same-sex subordinate (grey bars) compared with the proportion expected by chance (white bars). *P < 0.05; N ¼ individual thieves; error bars ¼ SE.

N2 ¼ 5, P ¼ 0.505) thieves stole significantly faster from a specific sex. Body Weight Dominance rank did not appear to affect the degree of weight loss (or gain) exhibited by adults during the winter dry season. There was no correlation between the weight change shown by an individual over the 10-week experimental period and the number of potential victims available to that individual, after variation between groups was taken into account (GLM: R2 ¼ 0.197, N ¼ 45, P ¼ 0.024; group: F3 ¼ 5.283, P ¼ 0.004; rank: F1 ¼ 0.661, P ¼ 0.421; sex: F1 ¼ 0.048, P ¼ 0.827; age: F1 ¼ 0.885, P ¼ 0.353). DISCUSSION Intrasexual competition appears to have played a major role in shaping patterns of interference foraging competition in female dwarf mongooses, but not in males. Nonalpha females commandeered the foraging excavations of same-sex subordinates (their life-long reproductive rivals) more often than those of male subordinates (Fig. 2a). Similarly, they targeted their nearest rival (the female directly below themselves in the hierarchy) more frequently than females of lower status (Fig. 2b), even though low-ranked

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individuals would presumably be easier to displace. However, these apparent preferences could conceivably be caused by differences in the availability of particular victims. For example, theft from same-sex subordinates would occur more often if same-sex individuals foraged together. We used a manipulation experiment to demonstrate that nonalpha females genuinely favoured samesex victims (Fig. 3) but the experiment failed to confirm their apparent preference for stealing from their immediate rivals. This discrepancy may have been due to the experiment's relatively small sample size (N ¼ 10) or could reflect the greater availability of close rivals as potential victims under natural conditions, due to either closer proximity (if littermates forage together, for example) or greater foraging efficiency. A thief's closest rival is also likely to be its oldest same-sex subordinate (because rank is positively correlated with age in dwarf mongooses; Creel, Creel, Wild, & Montfort, 1992) and, since foraging efficiency increases with age in many species (e.g. Sutherland, Jones, & Hadfield, 1986), this individual may unearth more prey (or more desirable prey; e.g. Barnard, 2000) than younger, low-ranking subordinates, making it available as a victim more frequently. However, if spatial proximity or age-related differences in foraging efficiency caused the disparity between the observational and experimental findings, we would expect male mongooses to also exhibit a bias for their immediate subordinates during natural prey theft. Clearly, in a species with such high reproductive skew, considerable benefit could be gained by reducing the competitive ability of same-sex rivals. This is particularly so for female dwarf mongooses, which not only suffer higher levels of intrasexual competition (Hauber & Lacey, 2005) but spend their entire lives competing with just a handful of individuals (their sisters and aunts). Such intense life-long rivalry for a very lucrative breeding role is likely to generate strong selection, favouring competitive traits such as the ability to capitalize on opportunities to intimidate competitors. Intense female rivalry in other social mammals is known to be associated with elevated female testosterone and aggression (Clutton-Brock, et al., 2006; Holekamp, et al., 1996; Reeve & Sherman, 1991), and our finding that female thieves ousted their victims more rapidly than did male thieves (regardless of the victim's sex) suggests that dwarf mongooses may also share this trait. It remains unclear whether the benefits attained by sex-biased thieves are limited to the reinforcement of their status or extend to include a nutritional component. Body weight appears to play a critical role in female competitive interactions in the social mongooses (Clutton-Brock, et al., 2006): in female dwarf mongooses, body size and weight are positively correlated with intragroup rank (Jooste, 2009), and in female meerkats weight (relative to competitors) is an important determinant of a female's ability to win and maintain dominance of a group (Hodge et al., 2008; Russell et al., 2004). It is not only ‘fighting weight’ that influences the outcome of femaleefemale competition for dominance in meerkats but also the relative weight of the competitors earlier in life (Hodge et al., 2008), and experiments have shown that meerkats adjust their food intake to ensure that their own weight matches that of their same-sex rivals (Huchard, English, Bell, Thavarajah, & Clutton-Brock, 2015). Additionally, once female meerkats attain dominance, they undergo a secondary period of growth (increasing in both weight and body length; Russell et al., 2004), and their tenure as dominant breeder is positively correlated with the degree of weight difference between themselves and their heaviest female subordinate (Clutton-Brock et al., 2006). In nonalpha female dwarf mongooses, changes in rank are mediated by severe fights, which normally take place after one female loses weight relative to its competitors (as a result of illness, injury or an attempt at breeding; Sharpe et al., 2013). Therefore, the

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2 *

*

1.8

Median level of success

1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0

Female (N = 11)

Male (N = 11)

Both (N = 22)

Figure 3. The median level of success (theft ¼ 2, share ¼ 1, no theft ¼ 0) shown by nonalpha dwarf mongooses in the manipulation experiments when interacting with victims of the same sex (grey bars) and the opposite sex (white bars). *P < 0.05. Box ¼ interquartile range; point ¼ median; whisker ¼ range.

6

Time to steal (s)

5 4 3 2 1 0

Female (N = 10)

Male (N = 9) Sex of thief

Figure 4. The mean time it took nonalpha mongooses to steal from their victims during the manipulation experiments. Error bars ¼ SE.

use of prey theft to exacerbate weight differences between rivals could have far-reaching benefits. Nevertheless, our study found no evidence that higher ranking mongooses (which have more opportunity to steal) suffered less weight loss over the experimental period than did lower ranking individuals. Our findings may have been confounded by the mild winter, however, as none of the study animals exhibited the degree of weight loss usually observed during winter (L. L. Sharpe, personal observation). None the less, it appears unlikely that the primary motivation for prey theft by nonalpha female mongooses was the reduction of their competitors' food intake, because they did not steal any more frequently than nonalpha males (Fig. 1). In fact, it is possible that female mongooses are precluded from adopting such a strategy by inclusive fitness costs (Young & Bennett, 2013), given that close female rivals are usually full siblings.

In marked contrast to nonalpha females, alpha female dwarf mongooses showed no bias for same-sex victims and stole prey indiscriminately from all group members. Once a female dwarf mongoose has attained alpha status, she holds the position for life (regardless of advanced age and/or debilitation; Rasa, 1987) and she uses endocrine mechanisms (enforced through infanticide; Creel, et al., 1992) to suppress the reproduction of subordinates. As a consequence, she has little to gain from depriving female subordinates of food. The high rate of prey theft shown by alpha females (four times that of nonalphas; Fig. 1) presumably reflects the heavy nutritional demands imposed by breeding, and is consistent with the behaviour of dominant female meerkats (Flower, 2007). The intense intrasexual competition characteristic of singular cooperatively breeding species appears to have strongly shaped patterns of foraging competition in nonalpha female dwarf mongooses, but it is not known whether other taxa also behave in this way. In many group-living mammals, high-ranking females enjoy a better diet and exhibit greater reproductive success than low-ranking females, presumably as a result of interference foraging competition (reviewed in Stockley & Bro-Jorgensen, 2011). Research on foraging competition in primates strongly supports this interpretation: for example, high-ranking female white-faced capuchin monkeys, Cebus capucinus, consume more food per hour than do subordinate females, and rates of feeding by subordinates (but not dominants) drop significantly as rates of intragroup aggression increase (Vogel, 2005). Yet, despite numerous studies of different primates (Isbell, 1991), it is still unknown whether female primates strategically target their reproductive rivals during foraging competition or simply harass subordinates indiscriminately. In spotted hyaena cubs, twins compete aggressively for milk and meat, even to the point of siblicide (Frank, Glickman, & Licht, 1991). Some studies (Golla, Hofer, & East, 1999) have found that rates of aggression between same-sex twins are higher than those between opposite-sex twins, particularly in all-female litters (as sisters remain close rivals for life), but these sex biases have not been

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detected in other studies (Smale, Holekamp, Weldele, Frank, & Glickman, 1995; Wahaj & Holekamp, 2006). Similarly, a study of interference competition in juvenile meerkats (which fight with littermates for access to provisioning adults) found that pups do not discriminate between competitors on the basis of sex (Hodge, Thornton, Flower, & Clutton-Brock, 2009). Although interference foraging competition has been extensively studied in birds (Vahl, Lok, van der Meer, & Piersma, 2005), there is limited information available regarding the targets of interference. Nevertheless, bartailed godwits, Limosa lapponica, are known to displace same-sex conspecifics more frequently than opposite-sex conspecifics, but this appears to be a product of the species' sex-specific niche segregation (i.e. the sexes feed in different microhabitats, so birds encounter same-sex individuals more often; Both, Edelaar, & Renema, 2003). Green woodhoopoes, Phoeniculus purpureus, also indulge in more than twice as many intrasexual displacements as intersexual displacements when foraging, with dominant birds aggressively excluding subordinates from prime feeding areas. Although this cooperatively breeding species does exhibit some sex-specific resource partitioning, individuals are significantly more likely to forage within 1 m of an opposite-sex group member, ruling out proximity as the cause for their preference for same-sex targets (Radford & Du Plessis, 2003). Only one previous study (of prey theft in cooperatively breeding meerkats) has directly tested whether individuals selectively target their reproductive rivals during foraging competition (Flower, 2007). Although meerkats are closely related to dwarf mongooses and the two species share a similar social structure and foraging behaviour (Clutton-Brock et al., 2006; Doolan & Macdonald, 1996; Rasa, 1973; Rood, 1986), Flower (2007) found no evidence of meerkats favouring same-sex victims. Experiments showed that dominant females are more likely to succeed when stealing from female victims (presumably because subordinate females fear eviction; Kutsukake & Clutton-Brock, 2006), but they did not preferentially target female subordinates. In fact, under natural foraging conditions, nonalpha meerkats attempted to steal prey significantly more often from opposite-sex victims than from samesex victims (Flower, 2007). This surprising reversal in the sex bias of thieves appears to be associated with differences in the two species' dominance systems. Although both meerkats and dwarf mongooses show agerelated (and to a lesser extent weight-related) dominance relationships (Creel et al., 1992; Sharpe, 2005; Thavarajah, Fenkes, & Clutton-Brock, 2014), two-thirds of the agonistic interactions occurring between nonalpha meerkats are competitive (i.e. involve mutual hip slamming with no outright winner) rather than directional (Sharpe, 2005). Such competitive interactions are rarely seen among dwarf mongooses, which establish a strict hierarchy, by fighting, at approximately 4e5 weeks of age (L. L. Sharpe, personal observation.). This species difference is particularly apparent after the death of an alpha female: in meerkats, the group's subordinate females fight viciously to ascertain the new alpha (Clutton-Brock, et al., 2006), whereas in dwarf mongooses the beta female simply assumes the alpha role without aggression (Rasa, 1987). The dwarf mongoose's despotic dominance hierarchy dictates the outcome of any contest between group members, so thieves suffer no potential cost (i.e. risk of aggression) when stealing from subordinates. In contrast, meerkats, lacking such a strict hierarchy, use ‘ownership rules’ (Maynard Smith & Parker, 1976) to dictate the outcome of disputes over food (Clutton-Brock & Huchard, 2013b; Flower, 2007) and only 12% of attempted prey thefts (even by the group's alpha female) are successful (Flower, 2007). Meerkats clearly suffer a real risk of their attempted thefts escalating into costly aggression, and this risk is likely to be exacerbated by the

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species' intense intrasexual competition (Clutton-Brock, et al., 2006), thus explaining why nonalpha meerkats are reluctant to initiate prey theft with same-sex group members. It is generally thought that the dominance relationships exhibited by female social mammals are shaped by competition over food, which is influenced in turn by the distribution of food sources (i.e. the abundance and degree of clumping and ‘monopolizability’ of food items; Sterck, et al., 1997). However, as the diet and foraging behaviour of meerkats and dwarf mongooses are very similar (Doolan & Macdonald, 1996; Rasa, 1973), it seems more likely that the difference in dominance styles is a product of female eviction, which is perpetrated by alpha female meerkats (CluttonBrock, et al., 1998) but not dwarf mongooses (Rasa, 1987). Unlike dwarf mongooses, subordinate female meerkats gain little from fighting to establish rank with rivals which may ultimately be evicted prior to the dominancy falling vacant. However, regardless of the cause, it is clear that relatively subtle differences in a species' social structure can significantly alter the way in which intrasexual competition is expressed. In conclusion, our study is the first to demonstrate that highranking individuals strategically target their reproductive rivals when embarking on interference foraging competition. These findings support the tenet that the intense intrasexual competition suffered by females within ‘singular’ cooperatively breeding species results in the differential development of competitive traits in females compared with males. Acknowledgments We thank the National Research Foundation (Grant no. SPF200805120002), Claude Leon Foundation and Bryan Guinness Charitable Trust for funding, Phuza Moya Private Game Reserve for permission to work in the reserve and accommodation, Billy Smith for accommodation and Tim Clutton-Brock for feedback on the manuscript. References Abbott, D. H. (1984). Behavioural and physiological suppression of fertility in subordinate marmoset monkeys. American Journal of Primatology, 6, 169e186. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227e267. Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton University Press. Andersson, M. (2004). Social polyandry, parental investment, sexual selection and evolution of reduced female gamete size. Evolution, 58, 24e34. Barnard, A. J. (2000). Costs and benefits of group foraging in cooperatively breeding meerkats. Cambridge, U.K.: University of Cambridge (Doctoral dissertation). Both, C., Edelaar, P., & Renema, W. (2003). Interference between the sexes in foraging bar-tailed godwits, Limosa lapponica. Ardea, 91, 268e272. Burland, T. M., Bennett, N. C., Jarvis, J. U. M., & Faulkes, C. G. (2002). Eusociality in African mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis). Proceedings of the Royal Society B: Biological Sciences, 269, 1025e1030. Cant, M. A., Hodge, S. J., Bell, M. B. V., Gilchrist, J. S., & Nichols, H. J. (2010). Reproductive control via eviction (but not threat of eviction) in banded mongooses. Proceedings of the Royal Society B: Biological Sciences, 277, 2219e2226. Clutton-Brock, T. H. (2009a). Sexual selection in females. Animal Behaviour, 77, 3e11. Clutton-Brock, T. H. (2009b). Structure and function in mammalian societies. Philosophical Transactions of the Royal Society, B, 364, 3229e3242. Clutton-Brock, T. H., Brotherton, P. N. M., Russell, A. F., O'Riain, M. J., Gaynor, D., Kansky, R., et al. (2001). Cooperation, control and concession in meerkat groups. Science, 291, 478e481. Clutton-Brock, T. H., Brotherton, P. N. M., Smith, R., McIlrath, G., Kansky, R., Gaynor, D., et al. (1998). Infanticide and expulsion of females in a cooperative mammal. Proceedings of the Royal Society B: Biological Sciences, 265, 2291e2295. Clutton-Brock, T. H., Hodge, S. J., Spong, G., Russell, A. F., Jordan, N. R., Bennett, N. C., et al. (2006). Intrasexual competition and sexual selection in cooperative mammals. Nature, 444, 1065e1068. Clutton-Brock, T. H., & Huchard, E. (2013a). Social competition and selection in males and females. Philosophical Transactions of the Royal Society, B, 368, 20130074.

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