Group size composition and reproductive success in wild common marmosets (Callithrix jacchus).код для вставкиСкачать
American Journal of Primatology 35311417 (1995) Group Size, Composition, and Reproductive Success in Wild Common Marmosets (Callithrixjacchus) A. KOENIG Institute of Anthropology, University of Gottingen, Gottingen, Germany Data from published sources about size and composition of wild common marmoset groups (Cullithrixjacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:l juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. o 1995 Wiley-Liss, Inc. Key words: group size, number of adult males, reproductive success, fitness benefits, Callithrix jacchus INTRODUCTION In the wild, South American callitrichid monkeys typically live in groups of three to 15 individuals and can be sociographically described as polygynandrous [Ferrari & Lopes Ferrari, 1989; Sussman & Garber, 1987; Rothe & Darms, 19931. Although the reproductive strategy is not yet fully known, callithrichids exhibit a flexible mating system including monogamy, polygyny, polyandry, and polygynandry [Ferrari & Lopes Ferrari, 1989; Sussman & Garber, 19871. Two behavioral traits characterize the Callithrichidae: (1) mature offspring of either sex may remain in the natal home range and delay their breeding [Goldizen & Terborgh, 19891, (2) all group members take part in alloparental care of the infants (mostly twins) of a single breeding female [Mittermeier et al., 1988; exceptions from a single female breeding reviewed in Koenig, 19921. Received August 23, 1994;revision accepted August 26, 1994. Address reprint requests to Andreas Koenig, Institute of Anthropology, University of Gottingen, Burgerstr. 50, 37073 Gottingen, Germany. 0 1995 Wiley-Liss, Inc. 312 / Koenig Although rare among primates, delayed breeding and care for offspring of others are widespread phenomena among birds and mammals [Brown, 1987; Riedman, 19821. Comprehensive hypotheses have been posed to explain the benefits for the breeders to tolerate nonbreeders as well as for the adaptive value of helping [Brown, 1987; Emlen, 1991; Emlen & Wrege, 19891. For at least some species excellent evidence is available that the number of surviving infants is closely related to the number of nonbreeders [Florida scrub jays (Aphelocoma c. coerulescens),white-fronted bee-eaters (Merops bullockiodes);reviewed in Emlen, 19911. In these species, the adaptive significance for breeders tolerating nonbreeders is to enhance survivorship of infants, thereby increasing direct fitness of the breeding individuals [Emlen, 1991; “direct fitness” sensu, Brown, 19801. If nonbreeders are related to the young they help to rear, they gain from helping by increasing their indirect fitness [Emlen, 1991; Emlen & Wrege, 1989; “indirect fitness” sensu, Brown, 19801. In callithrichids it has been shown that nonbreeders relieve breeders in several ways. Compared with small groups, breeding members of large groups can reduce their carrying load [McGrew, 1988; Price, 1992; Rothe et al., 1993a; Tardif et al., 19901 and their amount of sentinel behavior [Koenig, 19921. In addition, groups of larger size may be more successful in defending feeding sites [Garber, 19881. Thus, on a proximate level, evidence exists of reduced costs due to sharing of alloparental care, predator detection, and resource defense. Suspected fitness benefits, however, have rarely been investigated. Although hardly comparable to free-ranging conditions, laboratory studies have failed to show an effect of group size on the number of infants either in cotton-top tamarins (Saguinus (0.)oedipus) [Price & McGrew, 19901 or in common marmosets (Callithrixjacchus) [Rothe et al., 1993bl. In a recent laboratory study, increasing group size in common marmosets led to decreasing time without vigilance, probably indicating enhanced safety and survivorship in large groups [Koenig, 19921. Direct testing as to whether number of offspring and group size are related has been done for wild S. mystax and S.fuscicollis only. There, the number of dependent offspring is significantly related to the number of adult males present in a group [Sussman & Garber, 1987; see also Garber et al., 19841. However, it is questionable to assume that conditions found in wild tamarins are simply transferable to wild marmosets. This is particularly so because of marked differences between the genera in group size, reproductive behavior, and ecological niches [compare Ferrari & Lopes Ferrari, 1989; Mittermeier et al., 19881. Here I address the questions of how groups of wild common marmosets (C. jacchus) are composed and whether or not the number ofjuveniles is closely related to group size. In particular, it is expected that (1)the number of juveniles is significantly higher in large groups than in small groups and/or (2) the number of juveniles is significantly positively correlated to group size. METHODS Data Selection Data were taken from published sources (see Table I). From those studies that provided successive counts of groups, only the first count was used. It must be mentioned, however, that complete independence of data could not be assured. Some studies provided data from the same area but from different years, so it is likely that the same groups contributed more than once to the data set. Only those data were included for which useful estimates of age-classes were given. As ageclasses sometimes varied between the different studies original data were transferred into a new classification. This breakdown of ages followed Stevenson and Reproductive Success in Common Marmosets I 313 TABLE I. Size and Composition of Wild Common Marmoset Groups No. of group members Group/place Older than 5 Adult Adult SubTotal months Adult females males adult Juvenile 5 2 3 2 4 1 1 1 2 7 7 8 5 6 7 2 3 3 1 2 1 1 1 2 4 2 1 1 B/Tapacurab 8 7 6 ? ? I 1 CITapacurab 9 8 6 ? ? 2 1 EiTapacura Ea/Tapacura 10 10 8 8 3 5 1 1 2 4 5 3 2 2 NNlDois Irmaos".' BiTapacura" AITapacura" A/Tapacura AaITapacura 10 10 11 11 11 8 10 9 9 9 7 4 3 5 7 2 3 1 2 2 NNiTapacura".' CITapacura" Mean Range 12 13 9 12 3 4 4 4 2 4 3 1 8.7 3-13 7.3 3-12 7 8 4.4 2-8 1.8 1-4 2.5 1-5 2.9 1-6 1.4 0 -3 IIIlJo5.o Pessoa BlTapacura EITapacura" NNIJoBo Pessoa 3 5 6 6 3 UJo5.o Pessoa D/Tapacura" EclTapacurab 4 5 3 3 Reference Maier et al. [19821 Hubrecht  Scanlon et al. [19881 Alonso & Langguth [19891 Maier et a]. [19821 Scanlon et al. [ 19881 Stevenson & Rylands [ 19881 Stevenson & Rylands [19881 Stevenson & Rylands [19881 Hubrecht  Stevenson & Rylands [19881 Dixson et al.  Scanlon et al.  Scanlon et al. [19881 Hubrecht  Stevenson & Rylands Ll9881 Dixson e t al. I19921 Scanlon et al.  'Data from captures. bMinimum counts. 'Age classification of juveniles according to weight [compare Kuester, 19771. Rylands , but was restricted to three classes: adult (older than 15 months), subadult (younger than 15 but older than 5 months), juvenile (5 months and younger). Counts used in this study excluded groups containing more than one breeding female. Statistical Testing To test for relationships between the numbers of juveniles and the number of other group members Kruskal-Wallis ANOVA [Siegel, 19561 and Spearman rank correlation coefficient [one-tailed; Siegel, 19561were calculated using StatSoft CSS (Complete Statistical Software). RESULTS Of the published sources, data from 18 groups could be used and in 16 groups distinction between adult females and males was possible (Table I). Mean group size was 8.7 individuals, subdivided into 7.3 individuals older than 5 months and 1.4 juveniles. Mean number of adults was 4.4, including 1.8 adult females and 2.5 adult males. At least one adult female and one adult male lived in each group, but 314 / Koenig in only three of 18 groups was there a single adult pair (16.7%). Most groups contained one (N=8, 50.0%) or two adult females (N=5, 31.3%), and only three groups (18.8%) contained more than two adult females. In five groups only one adult male was present (31.3%), five groups contained two adult males (31.3%), and finally in six groups three to five adult males were present (37.5%). The number of subadults varied between one and six individuals, with a mean of 2.9. In all but two groups, there was at least one juvenile present and in one group there were even three. This unusual case was not the result of two females breeding, but according to DNA fingerprinting analysis, seems to be the first known case of triplets reared in the wild [Dixson et al., 19921. Statistical testing revealed no significant differences in the number of juveniles with regard to the number of other group members (Table 11; Kruskal-Wallis ANOVA). Correlational analysis revealed a significant positive correlation between the number of juveniles and the number of adult males (P < 0.01). The positive correlation between the number of juveniles and the number of individuals older than five months just failed to reach statistical significance (0.1 > P > 0.05).Examination of Table I1 suggests that twin juveniles were most often present if the groups contained at least three adult males. A post-hoc analysis of groups containing one or two adult males (mean: 1.1juveniles) vs. groups containing three or more adult males (mean: 2.0 juveniles) revealed a significant difference between these two classes with regard to the number of juveniles (Mann-Whitney U test, one-tailed [Siegel, 19561: n, = 10, n2= 6, U = 11.5, P < 0.02). DISCUSSION At the outset it should be emphasized that the results presented here must be viewed as preliminary because of the nature of the data set. Although successive counts of the same groups in the same year were not used, it is possible that the same groups were counted more than once in different years. Furthermore, the sample was not entirely drawn from one population and the data lack consistent information about habitat quality as well as rearing experience of breeders. Hence, it remains open whether there are multivariate dependencies between group size, habitat quality, rearing experience, and reproductive success [Emlen, 19911. With these caveats in mind, however, this is the first study to show that in common marmosets the number of juveniles is associated with the number of adult males. If one suggests that this correlation expresses real differences in reproductive success, breeding females in wild common marmosets would accrue direct fitness benefits from an increasing number of adult males present in a group. The respective conclusion for breeding males depends on their reproductive strategy. In strict monogamy, breeding males would realize the same fitness benefits as breeding females. If, however, reproduction in groups with more than one adult male would be truly polyandrous there would be no direct fitness benefits from an increase of the number of surviving offspring. In this case, related adult breeding males would get indirect fitness benefits from the reproductive efforts of their relatives, but unrelated breeding males would not. Thus, if one suggests polyandrous reproduction by unrelated males to be an adaptive strategy in common marmosets, it has to be asked whether polyandrous males receive other fitness benefits, e.g., improved direct fitness in the future due to improved survival [Emlen, 19911. If adult males are nonbreeding and related to the breeders, they would accrue future indirect fitness benefits from increased survivorship of the young and the young’s later efforts at breeding [Emlen, 1991; Emlen & Wrege, 19891. The same might be true for nonbreeding adult females or subadults. The data suggest, how- Reproductive Success in Common Marmosets / 315 TABLE 11. Relationship Between the Number of Juveniles and the Number of Other Group Members in Wild Common Marmoset Groups Statistical significance No. of other group members 2 - - 0.0 1.0 1.3 1.0 1.0 1.8 2.3 0.0 - - (11 (1) (3) (I) (2) (4) (4) (1) - (1) 3 4 5 6 9 1 7 8 10 11 12 Kruskal-Wallis Spearman ~ Mean no. of juveniles per no. of individuals older than 5 months (no. ofgroups) Mean no. of juveniles per no. of adult individuals (no. of groups) - 1.0 1.4 0.5 2.0 1.0 2.3 1.0 - (3) (51 (2) (2) (2) (3) (1) - 1.0 - - - - - - - - Mean no. of juveniles per no. of adult females (no. ofgroups) 1.4 1.6 1.5 1.0 - - - - - - - (11) (5) (2) (1) - - - - - - - - Mean no. of juveniles per no. of adult males (no. ofgroups) 0.8 1.4 2.0 2.0 2.0 (5) (5) (1) ( 3 ) (2) - - - - - - - - - - - Mean no. of juveniles per no. of subadult 1.0 2.0 1.5 1.3 2.0 1.0 - - individuals (no. ofgroups1 (5) (3) (4) ( 3 ) (1) (2) - - - - - - - - - 0.2>P>0.1 0.353 (O.l>P>O.05) 0.2>P>0.1 0.297 (0.2>P>O.l) 0.9>P>0.8 -0,001 (0.6>P>0.5) 0.3>P>0.2 0.607 (P<O.Ol) 0.6>P>0.5 0.123 (0.4>P>0.3) - - - ever, that their presence is not associated with a higher number of juveniles. Thus, questions remain to be answered as to whether or not these individuals really do help, i.e., provide fitness benefits [compare Emlen, 19911, why adult females delay breeding, and why they are tolerated. These questions become more complicated if nonbreeding group members are not related. Compared with existing data on tamarins this study shows apparent similarities between common marmosets and tamarins of the genus Saguinus. The mean number of adults, adult females, adult males, and the relationship between the number of adult males and the number of dependent young is virtually the same [compare Snowdon & Soini, 1988; Sussman & Garber, 19871. The general difference of group size between the genera stems from the different numbers of subadults, which is easily explained by the different reproductive outputs of common marmoset and tamarin females. Wild tamarin females mostly give birth one a year [Snowdon & Soini, 19881, whereas wild common marmoset females usually give birth twice a year [Stevenson & Rylands, 19881. Thus, although reproduction apparently differs between the genera, the key role of the number of adult males mediating the reproductive success of a given breeding female is the same. However, as the unanswered questions and the mere speculative nature of the discussion has shown, suggestions about the adaptive value of delayed breeding and helping behavior in callitrichids are far from being conclusive. Further progress depends on data becoming available to test the already existing hypotheses on fitness benefits of helping. 316 / K o e n i g CONCLUSION 1. In wild common marmosets the number of juveniles is significantly positively correlated t o the number of adult males. Groups containing one t o two adult males had significantly fewer juveniles than groups containing m o r e than two adult males. 2. With the presence of several adult males, breeding females seem t o gain direct fitness benefits due to an increased reproductive success. 3. Whether o t h e r group members realize fitness benefits depends on the reproductive s t r a t e g y of a d u l t males, their kinship, as well as the genetic relations h i p of nonbreeders to the offspring of the breeding individuals. ACKNOWLEDGMENTS I thank Carola Borries, E c k h a r d H e y m a n n , Bill McGrew, A n d r e a s P a u l , Ute Radespiel, Hartmut Rothe, and two anonymous reviewers for useful discussions and comments concerning this manuscript. The p a p e r is a reanalyzed and extended version of data presented in m y Ph.D thesis, which w a s supported by the German Research Council (DFG Ro 356/9-2). All the h e l p provided during the time of preparation is gratefully acknowledged. REFERENCES Alonso, C.; Langguth, A. Ecologia e comportamento de Callithrix jacchus (Primates: Callithrichidae) numa ilha de floresta Atlbntica. 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