Behavioral Ecology Advance Access originally published online on June 11, 2004
Behavioral Ecology 2004 15(6):952-960; doi:10.1093/beheco/arh071
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Pup escorting in the communal breeding banded mongoose: behavior, benefits, and maintenance
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Address correspondence to J. S. Gilchrist. E-mail: jsg24{at}cam.ac.uk.
Received 14 September 2003; revised 6 October 2003; accepted 21 October 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In cooperatively breeding species, helpers typically provide food to offspring, and distribute food throughout the brood or litter. However, in the communal breeding banded mongoose (Mungos mungo), some group members escort individual pups during their period of dependence, and escorts consistently associate with the same pup, although not all pups have an escort. The aim of the present study was to determine whether group members actively care for pups, pups benefit from association, and escorts or pups maintain association. Adult banded mongooses provision, protect, carry, groom, and play with pups. Although escorts fed pups more than did nonescorts, escorted pups were neither larger nor in better condition than were nonescorted pups at the end of the association period. Nevertheless, escorted pups were more likely to survive the association period than were nonescorted pups, providing evidence that carers confer beneficial effects on their recipients. However, the recipients are unlikely to be the genetic offspring of the escort because it is the pup that maintains the pup-escort association, and escorts, rather than showing a preference for provisioning their paired pup, follow a "feed the closest pup" rule. Although carers gain indirect fitness benefits through increasing survival of related pups, the lack of kin discrimination means carers are unable to maximize their fitness by preferentially escorting their own offspring or the offspring of closer relatives.
Key words: cooperative breeding, helpers, kin recognition, kin selection, Mungos mungo, nepotism, parental care, provisioning.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In most birds and mammals, carers have little opportunity but to raise their own offspring. However, in species that nest or den communally, or in which mixed paternity occurs, carers have the opportunity to raise offspring that vary in relatedness. In such species, natural selection would be expected to favor individuals that discriminate between young and provide care preferentially to those to which they are most related, thereby maximizing their evolutionary fitness (Hamilton, 1964
; Maynard Smith, 1964). However, although preferential care can occur (Lessells, 2002), nepotistic care is apparently absent in bird species that have mixed paternity (Kempenaers and Sheldon, 1996) and that lay communally (Craig and Jamieson, 1990; Koenig and Mumme, 1987; Koford et al., 1990). These observations suggest that, similar to social insects (Keller, 1997), vertebrates may be incapable of discriminating between offspring of different parentage within the same nest or den.
Although mechanisms of true kin recognition (rather than learning or using simple rules of thumb; see Grafen, 1990) are apparently absent in birds, they are present in at least some mammals (Heth et al., 2003; Mateo, 2002; Mateo and Johnston, 2000). In addition, although observations of preferential feeding in birds are largely restricted to nestling periods, observations of feeding preferences in mammals tend to be easier during the equivalent of the postfledgling period. The communally breeding banded mongoose (Mungos mungo) is unusual because carers commonly escort a single pup and direct their care almost exclusively to their paired pup. It is therefore an ideal species in which to investigate whether carers maximize kin selected benefits through preferentially directing care to offspring or close relatives.
The banded mongoose is a small (less than 2 kg), group-living carnivore, in which several males mate, and multiple females (up to 10; Gilchrist, 2001) regularly give birth together in the same den at the same time (Cant, 2000). After parturition, pups remain in the den for approximately 30 days, and group members baby-sit the pups (Cant, 2003). In the first few weeks after pups emerge from the den and follow the foraging group, most pups form stable associations with older group members (escorts; Cant, 1998).
In another paper, on the distribution of escorting behavior in banded mongooses (Gilchrist JS, Russell AF, in preparation), we show that escorting was costly to carers and that potential parents were responsible for the majority of escorting. The evidence for a cost to escorting prompts the following questions: what care do escorts contribute to pups, and do pups benefit from association with an escort? Having shown that parents account for the majority of escorting, it is important to evaluate whether they care for their own offspring. I therefore investigate whether escorts preferentially care for particular pups or if care is evenly distributed amongst the litter.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and population
Fieldwork was carried out from March 1997–February 2000, in an 8-km2 area, on and around Mweya peninsula, Queen Elizabeth National Park, southwest Uganda (0°12' S and 27°54' E). The vegetation of the study site was predominantly short and medium fire climax grassland, with numerous dense thickets dominated by Capparis tomentosa growing in association with Azima tetracantha and Euphorbia candelabrum (Lock, 1977
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The climate was equatorial, with little annual fluctuation in day length or temperature. Mean daily rainfall varied from 0–5.83 mm (mean = 2.16), and the proportion of days with rainfall varied from 0–0.73 (mean = 0.27). Food (invertebrate prey) availability is likely to increase with rainfall for all groups (Doolan and Macdonald, 1996; Waser et al., 1995), but three groups also had access to supplemental food from human garbage dumps (Gilchrist and Otali, 2002; Otali and Gilchrist, 2004). Groups are referred to as non–refuse-feeding or refuse-feeding, indicating their access to supplemental food.
Data were collected on a wild population of 10 groups of individually marked banded mongooses. Animals were classified in age classes as pups (0–90 days), infants (91–182 days), subadults (183–364 days), and adults (greater than 364 days). Group size (number of individuals aged more than 90 days) varied from three to 36 (overall mean = 13.6), and the number of emergent pups within a group varied from one to 18 (mean = 6.02) (Gilchrist, 2001). The availability of help was inferred from the ratio of adults (the age class responsible for the majority of escorting) to emergent pups, which ranged from 0.8:1–16:1 (mean = 3.3:1).
Data collection
Individuals were trapped, anesthetized, marked, and located by using methods outlined elsewhere (Cant, 2000; Cant et al., 2001). Pups were trapped during the association period. Head width (the zygomatic arch breadth: in millimeters ± 0.1) and weight (in grams ± 0.5) were measured, and the number of parasitic ticks on the belly was counted. Head width was used as an index of body size because of its strong correlation with age and minimal measurement error (Gilchrist JS, unpublished data). Animals were habituated to behavioral observation.
Pups were defined as emergent from the first visit when they were observed traveling with a foraging group (approximately 27 days after birth; Gilchrist, 2001). Groups with emergent pups were visited twice per day, once each morning and afternoon, and observed for at least 40 min. During each visit, all behavioral interactions between pups and other group members were recorded (all-occurrence continuous behavioral data; Martin and Bateson, 1993). On completion of observations, the observer qualitatively scored the presence (one) or absence (zero) of pup-escort association for each group member based upon proximity. Where a pup and group member (of 90 days old or more) were within 30 cm of each other, more than random, they were both scored as in association. This association score was a reliable summary of nearest neighbor scan data (Gilchrist, 2001). I compiled the association scores for every pup. Data were compiled for the entire association period of an emergent litter: from the date of emergence to the last date that pup-escort association was recorded for the litter. The association score (number of visits in association/number of visits) is a summary of the association frequency of each pup in each litter. In addition, association was qualitatively scored as strong, medium, and weak (Gilchrist, 2001).
Preliminary analysis of data suggested that the frequency of association declined from approximately 60 days of age. I therefore restricted subsequent analysis to data collected on pups no older than 60 days. Data on associations were collected on 150 pups, from 29 litters and 10 groups. Analyses using trapping data were based upon a reduced data set. The sample size for each analysis is stated in the text or after relevant tables (n = the total number of data points in an analysis).
Statistical analysis
Statistical analyses were performed by using Genstat 5.4.1 (Genstat, 1993). Normally distributed data were analyzed by using general linear models and restricted estimate maximum likelihood models (REMLs). Binomial data were analyzed by using generalized linear models, and iterated reweighted restricted estimate maximum likelihood models (IRREMLs), a robust form of generalized linear mixed model, with logit link function and binomial error distribution. REML and IRREML models enable the fitting of random terms and therefore account for repeated sampling across error terms (Schall, 1991): groups, litters, and individuals. The random terms (group identity, litter identity, and individual identity) were fitted whenever possible, but dropped from a model when identified as a negative component of variance (indicating that they explain none of the variance in the model). The general or generalized linear model procedure was used when all random terms were dropped from a model. Dispersion was estimated where dispersion was greater than one, and fixed at one where dispersion was less than one. Backward elimination was used in selecting fixed terms for the minimal model; except where terms were intercorrelated, in which case the forward procedure was used (Sokal and Rohlf, 1995). In the case of mean daily rainfall and proportion of days with rain, the term with the lower probability value was retained. Relevant two-way interactions were also tested (in the presence of the main effects) but are not included in results unless significant. The minimal model comprised only those parameters that contributed a significant amount to the explanatory power of the model. Chi-square and probability values for each significant fixed term were derived from each term fitted last in the minimal model with all significant terms in the model together, whereas values for nonsignificant terms were calculated from the minimal model with only that nonsignificant term added last. All tests were two-tailed with significance level p <.05. All means are expressed as ±1 SE.
Escort care
Do escorts actively care for pups? Consideration of interactive behavior between group members and pups restricted analysis to the adult age class because adults contributed the most to escorting behavior (Gilchrist JS, Russell AF, in preparation). To investigate adult-pup interactions, all-occurrence continuous behavioral data from 10 litters in six groups was analyzed for relative occurrence rates of adult-pup behavior.
Do escorts provision more than do nonescorts? I counted the number of successful provisioning events by group members to emergent pups within the association period for each litter. I fitted the number of provisions by each group member to a Poisson error distribution by using IRREML. The sex, age-class, and escort status (escort or nonescort) of each group member were fitted as fixed terms. The infant age-class was excluded because of low sample size. All-occurrence continuous data on provisioning was available on 151 group members from ten groups and 28 litters.
Are escorts more likely to initiate provisions than are nonescorts? The above analysis was repeated, restricting analysis to provisions initiated by the adult or subadult (and excluding provisions initiated by the pup).
Frequency and stability of association
Do male and female pups differ in their frequency of association with an escort? I fitted pup sex as a fixed term in an IRREML model. The number of visits in association with an escort was fitted to a binomial error distribution in which the denominator was the total number of visits between emergence and 60 days old. I fitted the following environmental terms as fixed effects: access to refuse, and rainfall in 60 days postemergence. I fitted the following social terms as fixed effects: group size, the number of pups from the previous cohort still surviving, the number of emergent pups, and the adult-to-pup ratio. Association data were available for 150 pups from 29 litters and 10 groups.
Do pups preferentially associate with male or female escorts? The number of visits in association with an adult male was fitted in an IRREML model to a binomial error distribution in which the denominator was the number of visits in association with an adult. The fixed effects fitted were the sex of the pup and the proportion of adults within the group that were male, and their interaction. In testing whether pups preferentially associated with male or female escorts, the results for analysis on all escorts, and analysis restricted to adult escorts were consistent. For simplicity I present the latter, as the majority of association was with adults (Gilchrist JS, Russell AF, in preparation). Association data were available for 150 pups from 29 litters and 10 groups.
Does the stability of association with an escort differ between male and female pups? Pup sex was fitted as a fixed term in a generalized linear model. The number of visits in association with the pup's most frequent escort was fitted to a binomial error distribution in which the denominator was the total number of visits with association between emergence and 60 days old. I also fitted environmental and social terms as for the analysis of frequency of association (above). Association stability data were available for 129 pups from 29 litters and 10 groups.
Pup size and condition
Do pups gain conditional benefits from association? To test whether pup size, weight, and tick count were correlated with association; each was fitted as the dependent variable in a model with association variables as fixed effects. The association variables fitted in each analysis were as follows: association index (number of visits with association/total number of visits), strong association index (number of visits with strong association score/total number of visits), proportion of visits with the pup's most frequent escort (number of visits in association with the pup's most frequent escort/total number of visits), and stability of association (number of visits with the pup's most frequent escort/total number of visits in association with an escort). In addition to fitting the sex of the pup as a fixed effect, I also fitted the sex of the pup's most frequent escort (female or male) and the age class of the pup's most frequent escort (adult or subadult). The following environmental terms were also fitted as fixed effects: access to refuse and rainfall in the 60 days before the date of trapping. The following social terms were fitted: group size, the number of pups from the previous cohort still surviving, the number of emergent pups, the number of adults, and the adult-to-pup ratio.
Analysis of pup size fitted pup head width as the response variable in a general linear model. I included the age of the pup as a fixed term. Analysis of pup condition fitted pup weight as the response variable in a REML model. I fitted the head width of the pup as a fixed effect to account for differences in size. Subsequent terms were therefore fitted to the individual's condition (weight adjusted for size). The time of day of trapping and the time between trapping and weighing were also fitted as covariates in the model but were omitted as nonsignificant. For analyses of pup size and condition, the fixed terms in the minimal model were subsequently rerun in a model with pup head width or weight from 19–33 days (restricted to the first trap date per pup), to test whether similar effects were apparent at emergence. Tick count was analyzed as the response variable in an IRREML model with a Poisson error distribution. I fitted pup age and head width as additional fixed effects.
Preliminary analysis on pup head width and weight showed that results of models run on all trapping data (multiple trap dates per pup) and on data restricted to the last trap date per pup (up to 60 days) were consistent. For simplicity, I therefore present the latter (also for tick data). Analysis was further restricted to pups with last trap date over 34 days of age, as pup-escort association was relatively rare before this age (Gilchrist JS, unpublished data). Size, weight, and tick data were available for 58 pups from 23 litters and 10 groups.
Pup survival
Is pup survival correlated with association? I fitted the association variables as fixed terms in an IRREML model. Pup survival (died = 0; survived = 1) during the period of reliable association (from 34–61 days) was fitted as the variable, to a binomial error distribution with denominator 1. I also fitted pup sex, head width, and weight at emergence, and environmental and social terms as for the analyses of pup size and condition. Survival and association data were available for 98 pups from 20 litters and nine groups.
Maintenance of association and preferential care
Do group members provision the closest pup? I counted all successful provisioning events, with respect to the distance of the provisioned pup relative to the provisioner (closest pup to the provisioner; not the closest pup to the provisioner).
Do escorts show a preference for provisioning the pup to which they were "paired" during a visit? I counted all successful provisioning events by escorts with respect to the initiator of the provision (the escort approached the pup; the pup approached the escort), whether the pup receiving the food item was the closest to the escort or farther than the closest pup, and whether the provisioned pup was the pup paired to the escort for the visit or was a pup that was not paired with the escort. All-occurrence continuous data of successful provisioning were available on 91 group members from 8 groups and 20 litters.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Escort care
Adults actively cared for pups in a number of potentially beneficial ways. Adults carried and provisioned pups and also initiated more groom and play bouts with pups than pups initiated toward adults (Table 1). Although pups were responsible for initiating more contacts, adults also initiated a substantial number of contacts with pups. However, adults were also aggressive to pups, in defense of a food item or potential food item (a scrape or hole that the adult was digging for food): of the 67 adult-to-pup defensive aggression events with known cause, 88% (59) were directly related to food, and the remaining 12% (8) were related to potential food items.
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Overall, escorts provisioned pups more than did nonescorts (female:
2 = 33.27, df = 1, p <.001, male: 2 = 39.32, df = 1, p <.001, n = 336) (Figure 1). Adults provisioned more than did subadults (2 = 4.02, df = 1, p =.045). However, individuals differed in their provisioning contribution according to escorting status and sex (escorting status x sex interaction: 2 = 4.98, df = 1, p =.026). Within escorts, there was no difference in provisioning between females and males, but among nonescorts, females provisioned less than did males (escorts: 2 = 2.10, df =1, p =.15, nonescorts: 2 = 12.47, df = 1, p <.001).
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The lower provisioning rate among nonescorts appears to be associated with an "un-willingness" to provision compared with escorts. The rate of provisions initiated by nonescorts was lower than that by escorts (female:
2 = 13.34, df = 1, p <.001, male: 2 = 8.96, df = 1, p <.001, n = 336) (Figure 1b). Although adults initiated provisions more than did subadults (2 = 8.54, df =1, p =.003), individuals differed in their provisioning contribution according to escorting status and sex (escorting status x sex interaction: 2 = 17.99, df = 1, p <.001). As for the analysis of overall provisioning rate, there was no difference in the rate of initiated provisions between the sexes within escorts, but female nonescorts initiated provisions less than did male nonescorts (escorts: 2 = 1.34, df = 1, p =.25, nonescorts: 2 = 9.04, df = 1, p <.003).
The higher provisioning rate of escorts was reflected in the frequency of provisions received by pups. Escorted pups were provisioned more than were unescorted pups: the number of provisions observed during the association period was positively correlated with the pup's association index (IRREML: 2 = 8.52, df =1, p =.004, n = 103).
Frequency and stability of association
Male and female pups associated with escorts at similar frequencies (0.52 ± 0.026, range = 0–0.60; pup sex 2 = 0.11, df = 1, p =.74, n = 150) (Figure 2). None of the environmental and social variables investigated were related to individual differences in the frequency with which pups were escorted.
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Pups showed no tendency to associate more with male or female escorts (the IRREML constant does not differ significantly from zero: 0.72 ± 0.58, n = 128), and this was consistent between male and female pups (pup sex x proportion of male adults interaction
2 = 0.09, df = 1, p =.77, n = 128).
Pups tended to form an association with a particular individual that was stable across visits, throughout the association period (proportion of escorted visits in association with a pup's most frequent escort: 0.79 ± 0.018, range = 0.25–1.00) (Figure 2b). The stability of association decreased with increasing group size (2 = 7.88, df = 1, p =.005, n = 127). None of the remaining environmental and social variables investigated were related to individual differences in the stability with which pups were escorted. However, group size and access to refuse are correlated (Gilchrist and Otali, 2002), and access to refuse was significant and negative when fitted alone in the IRREML model. I therefore reran the analysis separately for non–refuse-feeding and refuse-feeding groups to determine if the group size effect observed was independent of access to refuse. Group size was nonsignificant within both non–refuse-feeding and refuse-feeding groups. This suggests that the negative group size effect on stability of association may have been driven by access to refuse: pup association is less stable in refuse-feeding groups.
Pup size and condition
Escorted pups were not larger than nonescorted pups at peak association. Head width was positively correlated with mean daily rainfall in the previous 60 days and with the number of emergent pups (Table 2). None of the other terms included in the analysis affected head width. The significant terms from this analysis were included in an IRREML analysis of head width data for newly emerged pups. This showed that neither of the aforementioned effects was apparent at emergence.
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Escorted pups were not in better condition than were nonescorted pups at peak association. The proportion of days with rain in the previous 60 days was the only significant correlate of pup condition (
2 = 4.94, df = 1, p =.026, n = 58, correlation negative). The proportion of visits with the pup's most frequent escort was a marginally nonsignificant positive correlate (2 = 3.34, df = 1, p =.068, n = 58). None of the other terms tested were significant. I included rainfall and the proportion of visits with the pup's most frequent escort in an analysis of weight data for newly emerged pups: neither were significant. Similarly, analysis of tick counts found no effect of any measure of association: head width was the only significant positive correlate (2 = 44.5, df =1, p =.001, n = 62).
Pup survival
Of pups monitored from 34–60 days, 70 survived and 51 died. Of those that died, only one was visibly ill before disappearance, three were suspected to have been lost during intergroup encounters, one was killed by a warthog, and six were preyed upon by marabou storks. The remaining pups disappeared between visits with no known cause.
Survival of pups during the association period was positively correlated with association (Table 3). The proportion of visits with association recorded per pup was the most significant association measure correlated with individual survival. However, there was no additional advantage to stable association between visits (the proportion of visits in association with the pup's most frequent escort); pups that consistently associated with the same escort between visits had a similar survival rate to that of pups with low escort repeatability between visits. In addition, male pups had poorer survival than did female pups. There was also a marginally nonsignificant tendency for survival to increase with emergence weight. None of the other terms tested explained significant variation in individual pup survival (Table 3).
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Maintenance of association and preferential care
Pups actively maintained association with escorts: the pup followed the adult in 99% (1413/1433) of discrete follow records (Table 1). Pups also commonly sheltered under adults (Table 1), a behavior that probably confers protection because pups shelter when threatened by danger or by another pup. Moreover, pups also made contact with adults more often than adults made contact with pups: pups initiated 59% (700/1195) of contacts (Table 1).
In addition to maintaining association with their escort, pups also fought to defend access to older group members. The majority of pup-pup aggression was apparently for access to an escort: of 151 aggressive pup-pup encounters in which the cause of the interaction was known, 89% (134) were for access to an older group member (the remainder involved access to a potential food item).
The majority of pup escort-motivated aggression was in defense of the current escort. Of the escort-motivated aggressive interactions, 90% (119) were defense, in which the pup in a pup-escort pair was aggressive to another pup that was approaching its escort; the remaining 10% (13) were attacks, in which a pup approaching a pup-escort pair attacked the current associating pup. In the majority of cases, the aggressor won the interaction: 106 of the escort defenses were successful, with two draws, eight losses, and three of unknown result; in 10 of the 13 attacks the attacker won, and in the remaining three cases the attacker lost.
Group members tended to provision the nearest pup, 79% (753/950) of successful provisions were to the closest pup. Do escorts preferentially feed their paired pup or are they simply feeding the nearest pup? I found no evidence that escorts prefer to provision the pup with which they were associated on the visit: 79% (81/103) of escort-initiated provisions were to the closest pup, but 65% (53/81) of these were to pups that were not their "partner" for the visit. Of provisions to a distant pup, 73% (16/22) were to pups to which the escort was not paired. In contrast, only 35% (105/297) of pup-initiated provisions were to pups that were not the escort's partner (Figure 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The present study aimed to investigate how escorts care, whether pups benefit from association, and whether escorts preferentially care for specific pups. I have shown that banded mongoose adults care for pups by carrying, provisioning with food, grooming, and playing. Escorts provisioned more than did nonescorts, and they initiated more provisions than did nonescorts. Pup-escort associations were usually stable throughout the association period, and pups gained survival benefits from association. However, the pup (not the escort) actively maintained the pup-escort association by closely following and defending its escort from approach by other pups. In addition, escorts showed no preferential care and tended to provision the closest pup, irrespective of whether or not it was their paired pup.
Escort care
Adults actively provided care for pups: the most conspicuous types of adult-to-pup behavior were carrying and provisioning, but adults also contact, groom, and initiate play with pups. That escorts not only provisioned pups more than did nonescorts but also showed a greater willingness to provision (initiating more provisions than nonescorts) suggests that provisioning in the banded mongoose is not simply an instinctive response to a begging stimulus (see Jamieson, 1989).
Provisioning, in which group members leave, drop, or share a food item with a pup, represents a loss of food to the provider and also loss of time and energy in terms of foraging and handling the food item. Group members often do not provision when they have a food item, and escorts will refuse to provision and will even defend the item against the pup with which they are associating. This shows that adults do not necessarily feed pups, even when the pup approaches them giving a begging call (Gilchrist JS, personal observation), suggesting that provisioning can be costly. As escorts provision at higher rates than do nonescorts, they would therefore be expected to incur greater energetic costs. This appears to be the case because escorts lose more weight than do nonescorts over the escorting period (Gilchrist JS, Russell AF, in preparation). The lower willingness to provision by subadults may therefore reflect higher energetic constraints or lower foraging efficiency relative to adults.
Males were more likely to initiate provisioning than were females (within nonescorts). Sex differences in contributions to care may reflect differences in energetic constraints (Russell et al., 2003) or in the fitness benefits from provisioning pups (Clutton-Brock et al., 2002). Differences between the sexes in the amount of provisioning could be explained by differences in relatedness to the young or in uncertainty of parentage. For example, the provisioning effort of male dunnocks (Prunella modularis) is correlated with expected brood paternity (Davies et al., 1992). Alternatively, in species with sex-biased dispersal, the philopatric sex is likely to receive greater future benefits from provisioned young than is the dispersing sex, and this may explain why females provision more than do males in meerkats (Suricata suricatta; Brotherton et al., 2001; Clutton-Brock et al., 2002) and brown hyenas (Hyaena brunnea; Owens and Owens, 1984), and why males provision more than do females in most cooperative bird species (Cockburn, 1998). However, this is unlikely to be the case in banded mongooses because dispersal does not appear to be female biased (Cant et al., 2001; Gilchrist, 2001).
In noncooperative breeding species, parents may allocate resources differentially with regard to offspring sex, depending on the expected fitness returns from increasing the condition or survival of a particular sex (Lessells, 2002). The same rules apply to helpers in cooperative breeding systems, which should help the sex that will in turn provide the helper with the greatest inclusive fitness pay-off. In meerkats, females provision female pups more than male pups, whereas males provision pups of both sexes equally (Brotherton et al., 2001). A possible explanation for this is that females are both philopatric and "harder working" than are males, and therefore, greater future benefits are gained by helping to rear females (Clutton-Brock et al., 2002). In the banded mongoose, male and female pups are escorted at similar rates, and there is no bias in association toward male or female escorts. This suggests that there is no asymmetry in the fitness benefits accruing to either escorting sex with regard to the sex of the pup they escort (Lessells, 2002). Nor do pups gain better care or increased future fitness from associating with one sex over the other.
Is association stable?
The most striking difference between the banded mongoose and other cooperative breeding vertebrates is that young remain in stable association with individual group members. For example, whereas banded mongoose pups tend to consistently follow a single escort, meerkat pups wander between group members (Brotherton et al., 2001). That banded mongoose pups consistently follow a single escort is evidence that a single escort can supply sufficient food for a pup. In meerkats and many other cooperative species, this strategy is probably not possible because a single forager is incapable of supplying a pup with sufficient food, owing to either lower resource availability or higher energetic demands. Such stable one-to-one care of young is apparently unique, although there are some similarities with brood division in biparental and cooperative breeding bird species, in which each parent feeds a discrete subset of the brood (for a review of hypotheses, and tests based upon the white-browed scrub wren, Sericornis frontalis, see Leedman and Magrath, 2003).
Paired banded mongoose pups receive a much higher proportion of food items than do unpaired pups when they initiate the provision by approaching the adult, as they are usually the closest pup. Indeed, pups initiate a much higher frequency of provisions than adults. By intensively defending its escort against approach from other pups, a pup further increases the likelihood that it will be provisioned by the escort. By forming stable associations, pups potentially minimize pup-pup aggression. Indeed, Cant (1998) showed that pup-pup aggression was highest when pups first forage with the group, the period when pups are likely to be "sampling" potential escorts, and then rapidly dropped.
Pup-escort association was less stable in refuse-feeding than non–refuse-feeding groups. This may simply be owing to the larger group size and communal litter sizes of two of the refuse-feeding groups (Gilchrist, 2001; Gilchrist and Otali, 2002), resulting in increased pup-pup competitive interactions. Alternatively, variance in escort quality may be lower in refuse-feeding groups because escorts are generally in better condition owing to the supplementary food they receive from refuse feeding (Otali and Gilchrist, 2004), and therefore, pups may move between group members more.
Does escorting benefit the pups?
Helpers in cooperative breeding species commonly increase the growth and survival of young (Cockburn, 1998; Emlen, 1991; Hatchwell, 1999; Jennions and Macdonald, 1994), although such effects are not universal. Escorted banded mongoose pups are provisioned at a higher rate than are nonescorted pups, and pups probably also learn prey capture techniques faster by observing their escort (see Caldwell and Whiten, 2003). Escorting may additionally provide passive benefits to the pup; "sheltering" under the belly of an escort could provide protection from a rival pup or provide shade from the sun during foraging. However, despite these possible benefits, the size, condition, and parasite load of banded mongoose pups during the period of peak association were not correlated with association, although there was a tendency for pups in more stable association to be in better condition.
The higher survival of escorted pups is consequently unlikely to be caused by a lower probability of starvation. Indeed, only one pup that disappeared showed any sign of ill health. In cooperatively breeding birds, helpers have been shown to decrease predation of young (e.g., Innes and Johnston, 1996; Mumme, 1992; Rabenold, 1990). In the present study, the majority of cases of pup death in which the cause was known were owing to predation (also see Otali and Gilchrist, 2004). Escorts may provide protection from predators, because pups often shelter under the belly of their escort when danger threatens, and adults will carry young pups to safety. Banded mongoose pups that do not associate on a particular visit would be expected, on average, to be further from the nearest adult than is an escorted pup and therefore more vulnerable to predators. Pups that consistently associate are therefore likely to gain better protection and have a higher probability of survival to independence.
A possible alternative to predation explaining the higher mortality of unescorted pups is the risk of pups losing the group. Predation and losing the group have been suggested to be the two most significant causes of mortality among meerkat pups (Russell et al., 2002). Banded mongoose pups do sometimes become lost from their group, and this may occur more for unescorted pups that are generally further from an adult, as well as in refuse-feeding groups in which association is less stable.
Who maintains association: the escort or the pup?
Banded mongooses are plural breeders, with up to 10 females giving birth synchronously (Gilchrist, 2001), and numerous males involved in mate-guarding and mating (Cant, 2000). That escorting in the banded mongoose is costly (Gilchrist JS, Russell AF, in preparation) to the donors, and beneficial for the recipients (the present study), suggests that escorts should be selected to discriminate between pups and preferentially care for kin. The stability of pup-escort association suggests that selective care may occur.
However, it seems unlikely that parents preferentially direct care to kin. First, it is not the adult that is responsible for actively maintaining association. Pups maintain association by actively following adults. Pups also initiate contact with adults more than vice versa, commonly shelter underneath the belly of their escort, and aggressively defend their escort against approaches from other pups. Second, escorts show no preference toward provisioning the pup to which they are paired on a particular visit. Like meerkats, adults simply feed the closest pup (Brotherton et al., 2001; Manser and Avey, 2000). Feeding the nearest begging individual is similarly a general trend in both open nesting (Ostreiher, 2001) and single entrance nesting birds (Kacelnik et al., 1995).
Gilchrist JS and Russell AF (in preparation) show that potential parents escort more than do nonparents. However, if adults show no preference for provisioning specific pups, it is unlikely that kin recognition is in operation and therefore unlikely that escorts preferentially care for their genetic offspring or closer relatives. In this respect, banded mongooses are similar to other communal breeding vertebrate species in which females lay or give birth together in the same nest or den, and to species with mixed paternity and paternal care. In such breeding systems, in which young are mixed in a communal brood or litter, complex mechanisms of offspring recognition (e.g., based upon odor; Heth et al., 2003; Mateo, 2002; Mateo and Johnston, 2000) would need to evolve. The lack of a system of kin discrimination is probably owing to costs, and these could be exacerbated by selection on young to conceal their relatedness (Beecher, 1991; Johnstone, 1997; Keller, 1997).
That individuals are unable to identify kin when females give birth at the same time in the same place is supported by other observations. The survival of banded mongoose litters decreases with asynchronous parturition (Gilchrist, 2001). Asynchrony may provide information on maternity of young and enable individuals to reliably discriminate young and therefore commit infanticide (Gilchrist, 2001). Although discriminatory care is absent in species that give birth communally, in species in which females give birth separately but subsequently form communal crèches, mothers commonly selectively nurse their own offspring, as in spotted hyenas (Crocuta crocuta) and, to a lesser extent, lions (Felis leo) (Lewis and Pusey, 1997). Familiarity and learning could therefore play a role, one that cannot be realized in species with synchronous hatching or birth in a communal nest or den.
Conclusions
Pups maintain association, but it is unclear how pups choose their escort. In meerkats, the best provisioners are apparently the most successful foragers (Brotherton et al., 2001; Clutton-Brock et al., 2001, 2002). Foraging success may therefore contribute to the distribution of escorting in banded mongooses; that heavier individuals have higher escorting frequencies supports this (Gilchrist JS, Russell AF, in preparation). Analysis of group member foraging success is required to test whether the best foragers tend to be the best provisioners, and therefore escorts. Feeding potential escorts may also provide a good test of whether foraging efficiency limits provisioning (see Boland et al., 1997; Clutton-Brock et al., 2001, 2002; Eden, 1987; Wright and Dingemanse, 1999). Pups probably compete for and then defend reliable provisioners. This suggests a highly competitive system, in which dominant pups may be at a competitive advantage in securing access to a "good" escort and the benefits that come with it.
The absence of kin discrimination in banded mongooses does not mean that individuals fail to gain fitness benefits from care. On the contrary, most groups are comprised of relatives (Waldick RC, Gilchrist JS, Hodge S, Amos B, in preparation), and individuals will gain indirect fitness benefits by raising relatives (Russell and Hatchwell, 2001; Wright et al., 1999). In addition, escorts may gain future direct fitness benefits by increasing the size and work-force of the group (Clutton-Brock et al., 2002; Kokko et al., 2001).
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ACKNOWLEDGEMENTS |
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I would like to dedicate this article to the memory of my late father, Richard Gilchrist, for his encouragement and support of my interest in the natural world. I am extremely grateful to Andy Russell for insightful comments that greatly improved this manuscript. This article also benefited from the advice or comments of Tim Clutton-Brock, Tim Coulson, and two anonymous referees. I thank the Uganda Wildlife Authority for allowing me to conduct my research in Queen Elizabeth National Park, and Francis Mwanguhya and Emily Otali for providing invaluable assistance with data collection. For financial support, I thank the Biotechnology and Biological Sciences Research Council, the Ian Karten Charitable Trust, and in Cambridge: Magdalene College, the Board of Graduate Studies, the Cambridge Philosophical Society, and the Department of Zoology.
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