Effect of the enclosure on carriers' body weight loss in the cotton-top tamarin (Saguinus oedipus).код для вставкиСкачать
American Journal of Primatology 66:279–284 (2005) BRIEF REPORT Effect of the Enclosure on Carriers’ Body Weight Loss in the Cotton-Top Tamarin (Saguinus oedipus) SUSANA SÁNCHEZ1,2n, FERNANDO PELÁEZ1,2, ANA MORCILLO1, and CARLOS GIL-BÜRMANN1 1 Área de Psicobiologı´a, Facultad de Psicologı´a, Universidad Autónoma de Madrid, Madrid, Spain 2 German Primate Center, Göttingen, Germany Infant carrying in cotton-top tamarins is a costly activity that results in weight loss by the fathers and helpers. However, to date, measures of carrying costs have been obtained in small indoor enclosures. We studied body weight changes in adult and subadult individuals from eight large groups (n45) for 9 weeks after the birth of infants. Four groups were housed in large indoor/outdoor enclosures (42 m2 3.3 m high), and four were housed in small indoor enclosures (12 m2 2.4 m high). All of the individuals were weighed regularly at least three times a week. Reproductive males lost more weight in the big indoor/outdoor enclosures (mean=6.51%) than in the small indoor ones, as did male adult helpers (mean=5.59%) and female adult helpers (mean=4.4%). Still-growing subadult individuals also lost weight in the big indoor/outdoor enclosures (mean=3.17%), although the differences did not reach significance (P=0.07). These results support the hypothesis that cotton-top tamarins living in more natural settings experience higher weight loss than those housed under less-natural conditions. Am. J. Primatol. 66:279–284, 2005. r 2005 Wiley-Liss, Inc. Key words: enclosure effect; body weight loss; carrying costs; Saguinus oedipus INTRODUCTION In cotton-top tamarins (Saguinus oedipus), the fathers and adult and subadult individuals of both sexes (‘‘helpers’’) cooperate with the carrying of infants that represent 15% of the mother’s weight [Snowdon, 1996; Tardif et al., 1993]. Using data from saddle-back tamarins in the wild [Goldizen, 1987], Tardif Contract grant sponsor: MCyT-DGI; Contract grant numbers: PB-98-0094; BSO-2002-02611; Contract grant sponsor: Universidad Autónoma de Madrid/German Primate Center; Contract grant sponsor: Universidad Autónoma de Madrid; Contract grant number: FPU-2003. n Correspondence to: Susana Sánchez, Área de Psicobiologı́a, Facultad de Psicologı́a, Universidad Autónoma de Madrid, 28049 Madrid, Spain. E-mail: email@example.com Received 26 April 2004; revised 18 October 2004; revision accepted 7 February 2005 DOI 10.1002/ajp.20144 Published online in Wiley InterScience (www.interscience.com). r 2005 Wiley-Liss, Inc. 280 / Sánchez et al.  estimated that carrying two 30-day-old infants represents for an adult an increase of 21% in their energy expenditure. On the other hand, foraging and feeding time is reduced while carrying is performed [Price, 1992a; Tardif, 1994]. Sánchez et al.  found that after the birth of infants in indoor captive groups of cotton-top tamarins, fathers and male helpers lost weight, and this weight loss was related to their participation in carrying. The results also showed that tamarins’ feeding time and energy intake decreased while they were carrying infants, although no relation was found between these two variables and weight loss. In contrast, other studies showed that lactating mothers progressively gained weight as they reduced down their contribution to carrying, mainly during the time when a new pregnancy could take place (weeks 4–5) [Ziegler et al., 1990], and as a consequence of increased food intake [Kirkwood & Underwood, 1984; Price, 1992b; Sánchez et al., 1999]. Furthermore, Achenbach and Snowdon  found that after births occurred in cotton-top tamarin groups, the adult males also lost weight. However, in this case the weight loss was not found to be related to carrying time. When Achenbach and Snowdon  analyzed weight loss in adult males of different size groups, they observed that the loss was higher in small groups because infant carrying was shared by fewer individuals. Captive studies in which measures of carrying costs were obtained have been conducted in groups living in small indoor enclosures (e.g., 2 m2 by 2 m high enclosures: Anthropological Institute, University of Zürich (C. jacchus [Nievergelt & Martin, 1999]); 4 m2 by 2.2 m high enclosures at the Psychology Department, Wisconsin University (S. oedipus [Achenbach & Snowdon, 2002]; and 12 m2 by 2.4 m high enclosures at the German Primate Center, Göttingen (S. oedipus [Sánchez et al., 1999])). However, cotton-top tamarin groups in the wild occupy territories of 10.5–12.4 ha, most of which can be covered in 1–2 days [Savage, 1990]. We expect that in the wild, the effort of carrying infants will have a more dramatic effect on carriers’ weight loss. We predicted that even in captivity, but in a more naturalistic environment (i.e., large indoor/outdoor enclosures), carriers would lose more weight than in small indoor enclosures. MATERIALS AND METHODS Adult and subadult individuals from eight large groups (n45) of cotton-top tamarins were observed. During the study, mothers gave birth to 13 infants (five twin litters and three singleton litters). Juvenile individuals were excluded from the analysis because their contribution to carrying is very limited [Price, 1992c]. Four groups at the German Primate Center of Göttingen (DPZ), were housed in relatively small indoor enclosures (12 m2 2.4 m high) and kept at a temperature of 261C, humidity of 65%, and light length cycle of 12 hr. The other four groups were part of the tamarin colony at the Universidad Autónoma de Madrid (UAM) and were housed in indoor enclosures (3.5 m2 2.2 m high) at a temperature of 261C. The animals had continuous free access to exceptionally large outdoor areas (42 m2 3.3 m high) that were well furnished with branches and other enrichment elements. To avoid direct solar radiation, 80% of the outdoor areas were covered by shading nets. A system of automatic water sprinklers was placed outdoors to create mist to maximize cooling and humidity. The group sizes and compositions are listed in Table I. The weather conditions at the UAM colony are given in Table II. The breeding period of two groups (F and G) took place during spring, and the breeding periods of the other two groups took place in autumn (E) and in late autumn through early winter (H), respectively. Enclosure Effect on Carrier Weight Loss / 281 TABLE I. GROUP COMPOSITION of the Observed Families by Classes Classes Adult a Subadult Juvenile Group n Enclosure No.infants # ~ # ~ # ~ A B C D E F Gb H 13 10 8 6 8 8 8 10 DPZ DPZ DPZ DPZ UAM UAM UAM UAM 2 1 2 2 1 2 2 1 4 3 1 1 2 4 3 4 4 3 1 1 3 3 3 4 1 1 2 1 2 – 2 – 2 1 2 1 – 1 – – – 1 2 – 1 – – 1 2 1 – 2 – – – 1 a The adult males and adult females also include fathers and mothers, respectively. An adult female and a subadult male, who were included in this table, were expelled from the group before week 8 in the study. They were not included in the analyses for that reason. Adults, 424 months; subadults, 13–24 months; juveniles, 6–12 months [Price, 1991, 1992a]. b TABLE II. Weather Conditions at the UAM Colonyn Group RP Season M-min. M-max. M-daily M- H M-Sunshine E B N-B B N-B B N-B B N-B A-A W-W S-S W-W S-S W-S A-W A-A 5.5 1.6 7.4 3.6 11.6 4.9 4.5 6.4 14.9 15.7 17.9 18.6 24.2 16.9 11.1 18.1 10.35 7.9 12.7 10.7 18.1 10.6 7.6 11.9 14.5 13.8 16.3 16.7 22.3 15.1 10.1 16.8 58.5 48.8 54.3 45.0 47.6 50.8 68.9 49.7 10:20 10:16 13:35 11:08 14:28 12:19 9:27 10:42 F G H n RP, reproductive period; B, breeding (9 weeks); N-B, non-breeding (7 weeks). Season (onset-end of reproductive period): S, spring; A, autumn; W, winter. Temperature: M, mean (1C); M-, mean at 13’00 CET; H, humidity (%); M-sunshine, daily mean sunshine duration (hh:mm). UAM and DPZ used the same animal diets and feeding schedules, both of which were strictly controlled during the study to avoid body weight fluctuation caused by a variation in food supply. When infants were born, the groups were provided with proportional extra food. The animals had free, easy access to food placed indoors. Details regarding the diet, housing conditions, and feeding schedule at DPZ are provided elsewhere [Sánchez et al., 1999]. All of the groups were observed for 9 weeks following the birth of infants. This breeding period includes the infant total-dependence phase during the first 4 or 5 weeks [Kirkwood & Stathatos, 1992], when carrying costs are the highest [Sánchez et al., 1999], and the beginning of independence. In the 9th week, infants spend 50% of their time moving independently (in captivity [Price, 1992b] and in the wild [Savage et al., 1996]). All individuals were routinely weighed on a scale (71 g) (Sartorius Universal Type 46100) at least 3 times a week. The noninvasive procedure used was previously described by Sánchez et al. . To calculate weekly body weight changes, we subtracted the weekly mean weight from the prebirth weight (i.e., the weekly mean weight of the last week prior to birth). For reproductive females, their weight on the day infants were born was 282 / Sánchez et al. used as the prebirth weight. All groups were also weighed during nonbreeding periods (7 weeks). Nonparametric Mann-Whitney U-tests and Wilcoxon T-tests were used for most of the comparisons. Since we had predicted that after the birth of infants the tamarins in big indoor/outdoor enclosures would experience greater body weight losses, the Mann-Whitney U-tests for these analyses were one-tailed. A significance level of Po0.05 was considered for all analyses. RESULTS Before the births of infants, all of the reproductive males, adult helpers, and subadults at UAM weighed less than those at DPZ (mean=551.76777.80 g vs. mean=634.84773.63 g; U=135, n1=25, n2=25, Po0.001). To be sure that the difference in conditions between UAM and DPZ did not have an influence on weight changes in the absence of births, we compared body weight changes of adult tamarins in DPZ and UAM during a nonbreeding period of 7 weeks. No differences were found between the nonbreeding periods of the two colonies (U=108, n1=14, n2=21, P=0.18). On the other hand, although no differences were found in the weekly mean temperatures between breeding and nonbreeding periods at the UAM (U=439.5, n1=36, n2=28, P=0.38), individuals lost more weight during the breeding periods (T=13, n=21, Po0.001). During the breeding periods, temperatures were higher in the spring breeding periods than in the autumn-winter ones (U=46, n1=18, n2=18, Po0.001), but we found no differences when we compared weight losses (U=65, n1=12, n2=13, P=0.48). As Fig. 1 illustrates, when we compared the means of body weight losses after infant births in the two different locations, we found that reproductive males lost more weight in the UAM enclosures (mean= 6.51%73.4%) than in the DPZ ones ±Std.Dev. 6 ±Std.Err.Big indoor/outdoor enc. ±Std.Err.Small indoor enc. % Mean body weight change 4 Mean 2 0 -2 * ** ** -4 -6 -8 -10 Fathers Ad.Males Ad.Females Subadults Mothers Fig. 1. Body weight changes in fathers, adult male and female helpers, subadult helpers, and mothers in big indoor/outdoor enclosures and small indoor enclosures. Enclosure Effect on Carrier Weight Loss / 283 (mean= 2.2%72.88%) (U=2, n2=4, n1=4 P=0.04), and the same applied to adult male helpers (mean= 5.59%72.43% vs. mean= 0.88%70.36%) (U=1, n2=5, n1=9, Po0.01) and adult female helpers (mean= 4.4%71.88% vs. mean=0.48%71.19%) (U=0, n2=5, n1=8, Po0.01). In the case of subadults, we found the same tendency as before (mean= 3.17%74.26% vs. mean=1.15%75.12%); however, this result did not reach statistical significance (U=11, n1=4, n2=11, P=0.07). We also found no differences in mothers’ weight changes between the UAM and DPZ enclosures (mean= 0.14%73.68% vs. mean=1.33%73.36%) (U=7, n1=4, n2=4, P=0.38). DISCUSSION The results of this study support the notion that infant carrying in cotton-top tamarins is a costly activity, even in captive conditions, since both reproductive males and helpers experience weight loss after the birth [Sánchez et al., 1999]. We suggested that it would translate into higher body weight losses in the wild, and predicted that even in captivity–but in a more naturalistic environment, with big indoor/outdoor enclosures–carriers would lose more weight than carriers living in small indoor enclosures. Our results indicate that after the births of infants, fathers, adult male helpers, and adult female helpers experienced more weight loss in the UAM enclosures than in the DPZ ones (Fig. 1). The highest body weight losses were 16.85% for fathers, 20.23% for adult males, and 14.70% for adult females at the UAM enclosures. The fact that individuals weighed less at UAM than at DPZ before the births emphasizes the risk for higher relative weight losses in the more natural setting. Considering our results and those of Achenbach and Snowdon , one may conclude that even in captive environments, where food availability is guaranteed and there is no need to travel for foraging, both the number of individuals in the group and the characteristics of the enclosure are related to weight loss. The larger territory provided by the big indoor/outdoor enclosures of UAM may impose higher carrying efforts compared to the restricted conditions under which captive studies are usually conducted. Since abiotic factors, such as the length of day, temperature, and humidity, affect the time when callitrichids begin or cease activity (C. jacchus [Suchi & Rothe, 1999]), one could expect that these factors would also have some influence on the carrying efforts of tamarins in indoor/outdoor enclosures. Nevertheless, abiotic factors (such as temperature) did not appear to play a major role at the UAM colony. No differences were found in body weight losses between the spring breeding periods and the autumn-winter ones, despite the differences in temperature. In fact, outside temperatures at the UAM colony are far to be extreme, and animals can choose to go outside or remain indoors. In any case, all of these abiotic factors should have relatively little influence as long as nutritional resources are available [Suchi & Rothe, 1999]. A slight but not significant difference was found in the weight of mothers in the UAM and DPZ enclosures. Mothers tended to gain weight in small indoor enclosures, thereby improving their physical condition (Fig. 1) [Sánchez et al., 1999]. Mothers’ weight gain after birth has been related to low participation in carrying, and an increased food intake [Kirkwood & Underwood, 1984; Nievergelt & Martin, 1999; Price, 1992b; Sánchez et al., 1999], mainly when they can become pregnant again in weeks 4–5 after birth [Sánchez et al., 1999]. However, the lactating mothers in the large indoor/outdoor enclosures at UAM did not gain body weight as they did at DPZ. 284 / Sánchez et al. In conclusion, this study supports the idea that in a more naturalistic environment, carriers lose more weight than they do under the restrictive conditions of captivity, where most studies have been conducted. Although we still do not know the meaning of body weight loss in terms of its value as a selective force [Sánchez et al., 1999; Tardif, 1997], studies under semi-free conditions, including small groups, should provide data emphasizing the importance of cooperation for successfully coping with the high energy demands of infant carrying in callitrichids. ACKNOWLEDGMENTS We thank the primate breeding and husbandry staff of the DPZ and UAM for their technical assistance, and the anonymous referees for their very valuable comments and advice on the early version of this manuscript. REFERENCES Achenbach GG, Snowdon CT. 2002. Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int J Primatol 23:179–189. Goldizen AW. 1987. Facultative polyandry and the role of infant-carrying in wild saddleback tamarins (Saguinus fuscicollis). Behav Ecol Sociobiol 20:99–109. Kirkwood JK, Underwood DJ. 1984. 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