BRIEF REPORT

Effect of the Enclosure on Carriers’ Body Weight Lossin the Cotton-Top Tamarin (Saguinus oedipus)

SUSANA SANCHEZ1,2n, FERNANDO PELAEZ1,2, ANA MORCILLO1, and CARLOSGIL-BURMANN1

1Area de Psicobiologıa, Facultad de Psicologıa, Universidad Autonoma de Madrid,Madrid, Spain2German Primate Center, Gottingen, Germany

Infant carrying in cotton-top tamarins is a costly activity that results inweight loss by the fathers and helpers. However, to date, measures ofcarrying costs have been obtained in small indoor enclosures. We studiedbody weight changes in adult and subadult individuals from eight largegroups (n45) for 9 weeks after the birth of infants. Four groups werehoused in large indoor/outdoor enclosures (42 m2� 3.3 m high), and fourwere housed in small indoor enclosures (12 m2� 2.4 m high). All of theindividuals 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-growingsubadult 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 tamarinsliving in more natural settings experience higher weight loss than thosehoused 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; Saguinusoedipus

INTRODUCTION

In cotton-top tamarins (Saguinus oedipus), the fathers and adult andsubadult individuals of both sexes (‘‘helpers’’) cooperate with the carrying ofinfants 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 Autonoma de Madrid/German Primate Center; Contract grantsponsor: Universidad Autonoma de Madrid; Contract grant number: FPU-2003.

nCorrespondence to: Susana Sanchez, Area de Psicobiologıa, Facultad de Psicologıa, UniversidadAutonoma de Madrid, 28049 Madrid, Spain. E-mail: susana.sanchez@uam.es

Received 26 April 2004; revised 18 October 2004; revision accepted 7 February 2005

DOI 10.1002/ajp.20144Published online in Wiley InterScience (www.interscience.com).

r 2005 Wiley-Liss, Inc.

American Journal of Primatology 66:279–284 (2005)

[1997] estimated that carrying two 30-day-old infants represents for an adult anincrease of 21% in their energy expenditure. On the other hand, foraging andfeeding time is reduced while carrying is performed [Price, 1992a; Tardif, 1994].Sanchez et al. [1999] found that after the birth of infants in indoor captive groupsof cotton-top tamarins, fathers and male helpers lost weight, and this weight losswas related to their participation in carrying. The results also showed thattamarins’ feeding time and energy intake decreased while they were carryinginfants, although no relation was found between these two variables and weightloss. In contrast, other studies showed that lactating mothers progressivelygained weight as they reduced down their contribution to carrying, mainly duringthe 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; Sanchez et al., 1999]. Furthermore, Achenbach and Snowdon [2002]found that after births occurred in cotton-top tamarin groups, the adult malesalso lost weight. However, in this case the weight loss was not found to be relatedto carrying time. When Achenbach and Snowdon [2002] analyzed weight loss inadult males of different size groups, they observed that the loss was higher insmall groups because infant carrying was shared by fewer individuals.

Captive studies in which measures of carrying costs were obtained have beenconducted in groups living in small indoor enclosures (e.g., 2 m2 by 2 m highenclosures: Anthropological Institute, University of Zurich (C. jacchus [Niever-gelt & Martin, 1999]); 4 m2 by 2.2 m high enclosures at the PsychologyDepartment, Wisconsin University (S. oedipus [Achenbach & Snowdon, 2002];and 12 m2 by 2.4 m high enclosures at the German Primate Center, Gottingen(S. oedipus [Sanchez et al., 1999])). However, cotton-top tamarin groups in thewild 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 havea more dramatic effect on carriers’ weight loss. We predicted that even incaptivity, but in a more naturalistic environment (i.e., large indoor/outdoorenclosures), carriers would lose more weight than in small indoor enclosures.

MATERIALS AND METHODS

Adult and subadult individuals from eight large groups (n45) of cotton-toptamarins were observed. During the study, mothers gave birth to 13 infants (fivetwin litters and three singleton litters). Juvenile individuals were excluded fromthe analysis because their contribution to carrying is very limited [Price, 1992c].

Four groups at the German Primate Center of Gottingen (DPZ), were housedin relatively small indoor enclosures (12 m2� 2.4 m high) and kept at atemperature of 261C, humidity of 65%, and light length cycle of 12 hr. The otherfour groups were part of the tamarin colony at the Universidad Autonoma deMadrid (UAM) and were housed in indoor enclosures (3.5 m2� 2.2 m high) at atemperature of 261C. The animals had continuous free access to exceptionallylarge outdoor areas (42 m2� 3.3 m high) that were well furnished with branchesand other enrichment elements. To avoid direct solar radiation, 80% of theoutdoor areas were covered by shading nets. A system of automatic watersprinklers 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. Thebreeding period of two groups (F and G) took place during spring, and thebreeding periods of the other two groups took place in autumn (E) and in lateautumn through early winter (H), respectively.

280 / Sanchez et al.

UAM and DPZ used the same animal diets and feeding schedules, both ofwhich were strictly controlled during the study to avoid body weight fluctuationcaused by a variation in food supply. When infants were born, the groups wereprovided with proportional extra food. The animals had free, easy access to foodplaced indoors. Details regarding the diet, housing conditions, and feedingschedule at DPZ are provided elsewhere [Sanchez 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 4or 5 weeks [Kirkwood & Stathatos, 1992], when carrying costs are the highest[Sanchez 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 ascale (71 g) (Sartorius Universal Type 46100) at least 3 times a week. Thenoninvasive procedure used was previously described by Sanchez et al. [1999]. Tocalculate weekly body weight changes, we subtracted the weekly mean weightfrom the prebirth weight (i.e., the weekly mean weight of the last week prior tobirth). For reproductive females, their weight on the day infants were born was

TABLE I. GROUP COMPOSITION of the Observed Families by Classes

Classes

Adulta Subadult Juvenile

Group n Enclosure No.infants # ~ # ~ # ~

A 13 DPZ 2 4 4 1 2 – 2B 10 DPZ 1 3 3 1 1 1 1C 8 DPZ 2 1 1 2 2 2 –D 6 DPZ 2 1 1 1 1 – 2E 8 UAM 1 2 3 2 – 1 –F 8 UAM 2 4 3 – 1 – –Gb 8 UAM 2 3 3 2 – – –H 10 UAM 1 4 4 – – 1 1

aThe adult males and adult females also include fathers and mothers, respectively.bAn adult female and a subadult male, who were included in this table, were expelled from the group before week8 in the study. They were not included in the analyses for that reason. Adults, 424 months; subadults, 13–24months; juveniles, 6–12 months [Price, 1991, 1992a].

TABLE II. Weather Conditions at the UAM Colonyn

Group RP Season M-min. M-max. M-daily M-[13] H M-Sunshine

E B A-A 5.5 14.9 10.35 14.5 58.5 10:20N-B W-W 1.6 15.7 7.9 13.8 48.8 10:16

F B S-S 7.4 17.9 12.7 16.3 54.3 13:35N-B W-W 3.6 18.6 10.7 16.7 45.0 11:08

G B S-S 11.6 24.2 18.1 22.3 47.6 14:28N-B W-S 4.9 16.9 10.6 15.1 50.8 12:19

H B A-W 4.5 11.1 7.6 10.1 68.9 9:27N-B A-A 6.4 18.1 11.9 16.8 49.7 10:42

nRP, 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-[13],mean at 13’00 CET; H, humidity (%); M-sunshine, daily mean sunshine duration (hh:mm).

Enclosure Effect on Carrier Weight Loss / 281

used as the prebirth weight. All groups were also weighed during nonbreedingperiods (7 weeks).

Nonparametric Mann-Whitney U-tests and Wilcoxon T-tests were used formost of the comparisons. Since we had predicted that after the birth of infants thetamarins in big indoor/outdoor enclosures would experience greater body weightlosses, the Mann-Whitney U-tests for these analyses were one-tailed. Asignificance level of Po0.05 was considered for all analyses.

RESULTS

Before the births of infants, all of the reproductive males, adult helpers, andsubadults 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 thedifference in conditions between UAM and DPZ did not have an influence onweight changes in the absence of births, we compared body weight changes ofadult tamarins in DPZ and UAM during a nonbreeding period of 7 weeks. Nodifferences 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 meantemperatures 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 higherin 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 afterinfant births in the two different locations, we found that reproductive males lostmore weight in the UAM enclosures (mean=�6.51%73.4%) than in the DPZ ones

% M

ean

body

wei

ght c

hang

e

-10

-8

-6

-4

-2

0

2

4

6±Std.Dev.

±Std.Err.Big indoor/outdoor enc.

±Std.Err.Small indoor enc.

Mean

Ad.MalesFathers Ad.Females Subadults Mothers

* ****

Fig. 1. Body weight changes in fathers, adult male and female helpers, subadult helpers, andmothers in big indoor/outdoor enclosures and small indoor enclosures.

282 / Sanchez et al.

(mean=�2.2%72.88%) (U=2, n2=4, n1=4 P=0.04), and the same applied toadult 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’ weightchanges 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-toptamarins is a costly activity, even in captive conditions, since both reproductivemales and helpers experience weight loss after the birth [Sanchez et al., 1999]. Wesuggested that it would translate into higher body weight losses in the wild, andpredicted that even in captivity–but in a more naturalistic environment, with bigindoor/outdoor enclosures–carriers would lose more weight than carriers living insmall indoor enclosures. Our results indicate that after the births of infants,fathers, adult male helpers, and adult female helpers experienced more weightloss in the UAM enclosures than in the DPZ ones (Fig. 1). The highest bodyweight losses were 16.85% for fathers, 20.23% for adult males, and 14.70% foradult females at the UAM enclosures. The fact that individuals weighed less atUAM than at DPZ before the births emphasizes the risk for higher relative weightlosses in the more natural setting.

Considering our results and those of Achenbach and Snowdon [2002], onemay conclude that even in captive environments, where food availability isguaranteed and there is no need to travel for foraging, both the number ofindividuals in the group and the characteristics of the enclosure are related toweight loss. The larger territory provided by the big indoor/outdoor enclosures ofUAM may impose higher carrying efforts compared to the restricted conditionsunder which captive studies are usually conducted. Since abiotic factors, such asthe length of day, temperature, and humidity, affect the time when callitrichidsbegin or cease activity (C. jacchus [Suchi & Rothe, 1999]), one could expect thatthese factors would also have some influence on the carrying efforts of tamarins inindoor/outdoor enclosures. Nevertheless, abiotic factors (such as temperature) didnot appear to play a major role at the UAM colony. No differences were found inbody weight losses between the spring breeding periods and the autumn-winterones, despite the differences in temperature. In fact, outside temperatures at theUAM colony are far to be extreme, and animals can choose to go outside or remainindoors. In any case, all of these abiotic factors should have relatively littleinfluence as long as nutritional resources are available [Suchi & Rothe, 1999].

A slight but not significant difference was found in the weight of mothers inthe UAM and DPZ enclosures. Mothers tended to gain weight in small indoorenclosures, thereby improving their physical condition (Fig. 1) [Sanchez et al.,1999]. Mothers’ weight gain after birth has been related to low participation incarrying, and an increased food intake [Kirkwood & Underwood, 1984; Nievergelt& Martin, 1999; Price, 1992b; Sanchez et al., 1999], mainly when they can becomepregnant again in weeks 4–5 after birth [Sanchez et al., 1999]. However, thelactating mothers in the large indoor/outdoor enclosures at UAM did not gainbody weight as they did at DPZ.

Enclosure Effect on Carrier Weight Loss / 283

In conclusion, this study supports the idea that in a more naturalisticenvironment, carriers lose more weight than they do under the restrictiveconditions of captivity, where most studies have been conducted. Although westill do not know the meaning of body weight loss in terms of its value as aselective force [Sanchez et al., 1999; Tardif, 1997], studies under semi-freeconditions, including small groups, should provide data emphasizing theimportance of cooperation for successfully coping with the high energy demandsof infant carrying in callitrichids.

ACKNOWLEDGMENTS

We thank the primate breeding and husbandry staff of the DPZ and UAM fortheir technical assistance, and the anonymous referees for their very valuablecomments and advice on the early version of this manuscript.

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