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Effects of Helpers on Juvenile Development and Survival in Meerkats

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Science  28 Sep 2001:
Vol. 293, Issue 5539, pp. 2446-2449
DOI: 10.1126/science.1061274

Abstract

Although breeding success is known to increase with group size in several cooperative mammals, the mechanisms underlying these relationships are uncertain. We show that in wild groups of cooperative meerkats, Suricata suricatta, reductions in the ratio of helpers to pups depress the daily weight gain and growth of pups and the daily weight gain of helpers. Increases in the daily weight gain of pups are associated with heavier weights at independence and at 1 year of age, as well as with improved foraging success as juveniles and higher survival rates through the first year of life. These results suggest that the effects of helpers on the fitness of pups extend beyond weaning and that helpers may gain direct as well as indirect benefits by feeding pups.

In social mammals whose young are reared principally by their parents and are rarely (or never) fed directly by other group members, competition for resources commonly increases in large groups, and breeding success either declines with increasing group size or shows no consistent relation to it (1, 2). In contrast, positive relations between breeding success and group size are common in social mammals whose young are reared by helpers (3–8). Although these correlations suggest that the presence of helpers benefits juveniles in cooperative species, the ecological and behavioral mechanisms underlying them are poorly understood, and group size could affect several different processes that influence juvenile survival, including predation, infanticide, and starvation (3).

Like other social mammals whose young receive much of their food from helpers, juvenile survival increases in larger groups of Kalahari meerkats, Suricata suricatta (9). This cooperative mongoose lives in groups of 2 to 30, consisting of a dominant male and female that are the parents of over 80% of young born in the group (10) and a variable number of helpers that assist in guarding and feeding young during their first 10 to 12 weeks of life (11, 12). All individuals over 3 months of age assist in feeding pups between the ages of 30 days (when they start to travel with the group) until approximately 90 days (when they forage independently), although the contributions to pup feeding of juveniles 3 to 6 months old are often small.

Across litters, both the amount of food that pups receive (Fig. 1A) and their rate of daily weight gain (Fig. 1B) (13) rise with the ratio of helpers to pups, which increases with group size (14). These correlations could, however, be a consequence of independent effects of territory quality on food intake rate, pup weight gain, and number of helpers (15). To determine whether the presence of helpers exerts a causal effect on juvenile development, studies of cooperative birds have removed a proportion of helpers (15,16). However, because manipulations of this kind may disrupt social relationships within the group, potentially affecting contributions to cooperative activities (16), we preferred to manipulate the ratio of helpers to pups by temporarily removing pups from or adding pups to litters (17). Our experiments show that increases in helper:pup ratios raise the rate of weight gain in pups (Fig. 2A), whereas reductions lower their rate of weight gain (Fig. 2B). Helpers fed introduced pups as frequently as the group's own pups (18), and reductions in helper:pup ratios also reduced the daily weight gain of helpers (Fig. 2D). Helpers feeding experimentally enlarged litters were probably responding to an increased frequency of begging calls given by unsatisfied pups, because hungry pups call more frequently and playbacks of pup begging calls raise the proportion of food items given to pups (19). In contrast, increases in helper:pup ratios did not lead to a significant increase in the rate of weight gain of helpers, though there was a nonsignificant trend in this direction (Fig. 2C).

Figure 1

Downstream effects of pup feeding by helpers on the daily weight gain of pups, their weight and foraging success at independence, and their weight at adulthood (13,14, 20). Analyses were conducted on means for 46 litters [(A) through (C)], 26 litters [(D) through (E)], and 35 litters (F) and controlled for the effects of repeated measures within eight groups. Axes with negative values depict residual values obtained from regressions of the variable in question on age. (A) Correlation between helper:pup ratios and mean rate of estimated food intake by individual pups between 35 and 75 days old, measured in grams per hour (F 1,37 = 21.31, P < 0.001). (B) Correlation between helper:pup ratios and mean daily weight gain of pups between 35 and 75 days old (F 1,37 = 12.74, P = 0.001). (C) Correlation between mean daily weight gain of pups between 35 and 75 days old and mean body weight of the same individuals at independence (3 to 4 months) (F 1,37 = 10.83, P = 0.002). (D) Correlation between mean daily weight gain of pups between 35 and 75 days old and mean body weight of the same individuals at adulthood (12 to 13 months) (F 1,17 = 5.73, P = 0.041). (E) Correlation between the weight of individuals at independence and the number of food items they find per hour at independence (F 1,17 = 8.6,P = 0.01). (F) Correlation between the body weight of pups at independence, after pup feeding by helpers had ceased, and their mean residual daily weight gain over the same period (F 1,26 = 7.29, P = 0.012).

Figure 2

Effects of manipulating helper:pup ratios (17) on daily weight gain of pups and helpers. In this experiment, helper:pup ratios were either temporarily increased by removing 75% of pups or were reduced by increasing litter size by 75%. Control values were mean measures of daily weight gain in pups and helpers in the same group within 2 days of the experiment. Analyses used paired t tests and one-tailed Pvalues are shown. n, number of temporary removals. (A) Pups in reduced litters (high helper:pup ratios) showed a 100% increase in their daily weight gain (t 9 = 3.86, P < 0.003) as well as in the number of items they received per hour (t 9 = 4.71, P < 0.001). (B) Pups in increased litters (low helper:pup ratios) showed a 45% reduction in their daily weight gain (t 8 = 3.65, P < 0.004) as well as a 34% reduction in items received per hour (t 8 = 2.81, P < 0.02). Resident pups in increased litters showed a 38% decrease in daily weight gain (t 8 = 2.22, P < 0.02) as well as a 32% reduction in items received per hour (t 8 = 1.57, P = 0.077). (C) Helpers feeding reduced litters showed a nonsignificant tendency for daily weight gain to increase as compared with values for the same individuals on the four previous days (t 9 = –1.24, P = 0.12). (D) Helpers feeding increased litters showed a significant reduction in their daily weight gain of 31% as compared with values for the same individuals on the four previous days (t 8 = 3.41, P < 0.005).

High rates of daily weight gain have beneficial consequences for the subsequent development of pups. Average rates of daily weight gain during peak provisioning (between 35 and 75 days after birth) are correlated with body weight at independence (3 to 4 months) (Fig. 1C) as well as at adulthood (12 to 13 months) (Fig. 1D) (20). These effects were confirmed by experimentally feeding pups (21): Individual pups that were fed with 12 g of egg twice per day during the period of pup feeding showed an average daily (12-hour) weight gain that was 7 g higher than that of unfed controls (F 1,19 = 11.40, P= 0.003) and were heavier as juveniles, subadults, and adults (at 3 to 4 months, F 1,20 = 5.29, P = 0.032; at 6 to 7 months, F 1,14 = 6.34,P = 0.025; at 12 to 13 months,F 1,6 = 9.42, P = 0.022). Pups that are relatively heavy at independence catch more food items (Fig. 1E) and show higher rates of daily weight gain (Fig. 1F). Finally, the rate of daily weight gain of pups during peak provisioning was consistently related to their survival between emergence and 12 months (Table 1). After daily weight gain is included, helper:pup ratios have no additional effect on pup survival, because their effects are absorbed by the inclusion of daily weight gain in the model. However, pup survival increases with group size when other effects are controlled for, possibly because the effectiveness of predator detection rises in large groups (9).

Table 1

Generalized linear mixed model of the factors associated with individual survival from burrow emergence (at approximately 18 days) to 1 year. Analysis was conducted on 135 individuals from 41 litters in eight groups using the program GENSTAT 5.4.1 (30). The data were fitted to a binomial error structure with logit-link function, and litter identity was fitted as a random term to control for repeated measures within litters (1–6). Probability of survival to 1 year was positively influenced by average group size between death or 1 year (whichever was soonest) and mean age-related weight gain during the peak pup provisioning period, although survivorship declined again in large groups. Daily weight gain was the hourly weight gain of pups during the morning feeding period between the ages of 35 and 75 days (or death). Individuals were only included in the model if they were born a year or more before the end of data collection.

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Our results show that the presence of helpers has substantial benefits for the daily weight gain, growth, and survival of meerkat pups. In small groups with low helper:pup ratios, helpers do not provide sufficient food to allow pups to maximize their growth rates, leading to reductions in their body weight and survival over the first year of life. The effects of helpers on early development and subsequent survival in meerkats and some other cooperative breeders (22) parallel the associations between maternal characteristics, early development, and adult fitness found in many other vertebrates (23). These results show that estimates of the effects of helpers on the survival of young to fledging or weaning are likely to underestimate the extent to which helpers affect the fitness of developing pups. Moreover, in addition to any indirect benefits gained by helpers assisting kin (24), these effects are likely to contribute to the direct fitness of the helpers themselves if foraging success or survival increase with group size (9, 10, 25, 26) or if the number or condition of pups raised reduces the efforts that individual helpers need to devote to raising subsequent litters (27, 28).

The contrasting relations between group size and breeding success found in social mammals whose young are fed by parents alone (1, 2) and those whose young are fed by parents and helpers (3–8) suggest that strong positive correlations between group size and breeding success may be confined to species, such as meerkats, in which young obtain much of their food from helpers or are dependent on them for some other resource. In contrast, when dependent young obtain most of their food from parents and little from helpers, the negative effects of increased group size on resource competition may offset the beneficial consequences of helpers, so that breeding success is unrelated or even negatively related to group size (29).

Differences in the extent to which breeding success and juvenile survival depend on group size have important implications for the population dynamics of social species (4,7). Where members of small groups show reduced survival and reproductive success, density-independent factors that reduce survival, local density, and group size may depress average breeding success and raise the frequency of group extinctions. The magnitude of these “Allee” effects (inverse density dependence) is likely to increase with the dependence of breeding success and survival on group size (4) and, as expected, recent studies of several cooperative breeders have revealed high rates of group extinction (4, 26).

  • * To whom correspondence should be addressed. E-mail: thcb{at}hermes.cam.ac.uk

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