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Correlates of molt in golden lion tamarins (Leontopithecus rosalia).

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American Journal of Primatology 36:277-284 (1995)
Correlates of Molt in Golden Lion Tamarins
(Leontopithecus rosalia)
JAMES M. DIETZ', ANDREW J. BAKER', AND TERILYN D. ALLENDORF3
1,3Departmentof Zoology, University of Maryland, College Park; 'Philadelphia Zoological
Garden, Philadelphia, Pennsylvania
In this paper we describe the timing and correlates of molt for a native
population of golden lion tamarins (Leontopithecus rosalia). We conducted
820 examinations of 267 adult tamarins over a 7.75 year period to determine the annual molting cycle in this population. Dorsal molt was a n
annual event for most individuals in the study population; however, 10%
of sampled individuals apparently molted twice in a 12 month period.
Duration of molt was estimated a t 5-6 weeks. The proportion of samples
in which tamarins were in molt was significantly greater during the wet
season than the dry season and positively correlated with mean monthly
precipitation and minimum temperature but not tamarin births, suggesting a n environmental component to timing of molt. We found no sex differences in the occurrence of molt during wet or dry seasons. However, the
relative frequency of samples in molt was significantly less for gravid
females than for nongravid females. In four polygynous groups, socially
dominant females gave birth before subordinate females, and younger
reproductive females completed molt before older reproductive females.
0 1995 Wiley-Liss, Inc.
Key words: molt, pelage, Callitrichidae, golden lion tamarin
INTRODUCTION
Hair, being nonliving material, is subject to considerable wear and leaching of
pigments and is replaced gradually or during periodic molts. The timing of molt in
many north-temperate mammal species has apparent adaptive significance relative to seasonal changes in the needs for insulation or protective coloration [e.g.,
Collins, 1923; Linzey & Linzey, 19671. In several species molt takes place in the
spring and fall, and summer pelage is less dense than winter pelage. In species
inhabiting areas with seasonal snowfall, winter pelage may differ in color from
summer pelage, possibly contributing to protection from predators or efficiency as
predators. Finally, pelage replacement necessitates the relatively expensive process of protein synthesis. Timing of molt in species like L. rosalia, in which the
energetic burden of reproduction is thought to be great [Leutenegger, 1980; Dietz
Received for publication October 28, 1993; revision accepted January 5, 1995
Address reprint requests to James M. Dietz, Department of Zoology, University of Maryland, College
Park, MD 20742.
0 1995 Wiley-Liss, Inc.
278 I Dietz et al.
et al., 1994; Tardif et al., 19931, should correspond with seasons of resource abundance.
Although patterns of seasonal molt have been well documented for other mammals [e.g., Ling, 19701, little is known about timing of molt in tropical taxa. To our
knowledge no systematic study of molt patterns has been published for any native
primate population. In this paper we describe physical and temporal patterns of
adult molt in a wild population of golden lion tamarins. We also examine population-level correlations of precipitation, temperature, and birth season and effects of
age, sex, and social rank with the occurrence of molt to evaluate the adaptive
significance of timing of molt in this population.
Previous reports of molt patterns in callitrichid primates were based on museum specimens or captive animals. Hershkovitz [1977, p. 831 reported no “molt
line” or “synchronized replacement” of fur for this family. He found no evidence of
a “distinct molt pattern” in L. rosalia [Hershkovitz, 1977, p. 8261. However, Coimbra-Filho and Maia [1979] described seasonal molt for a captive colony of L. rosalia
in Rio de Janeiro, Brazil. In that study, molt began in September, the month they
identified as the beginning of the birth season, and was delayed in pregnant females. These authors speculated that a hormonal mechanism influenced or determined the timing of molt.
Among other primates, Vessey and Morrison [1970] described molt patterns in
two introduced populations of rhesus monkeys (Macaca mulatta). In that study,
molt was a n annual event with adult males and nonpregnant females molting
before females with young of the year. Molt began at the end of the mating season
a t both study sites. However, molt began 3 months earlier a t the eastern site than
a t the western site, suggesting that hormonal factors related to reproduction influenced timing of molt.
METHODS
The study site was the 5,200 ha POGO
das Antas Biological Reserve, 70 km NE
of the city of Rio de Janeiro, Brazil. During the 7.75 years of this study (March,
1985, to January, 19931, we live-trapped and tattooed 267 adult golden lion tamarins. We defined adults as individuals weighing more than 500 g or with heavily
worn canine teeth or known by birthdate to be a t least 18 months of age. Many of
these animals were captured repeatedly. As part of a n overall examination, captured animals were chemically immobilized, examined for pelage characteristics,
and classified as in molt, between molts, or recently molted. Individuals defined as
in molt were those with a distinct dorsal molt line on the dorsal torso separating
new pelage from old pelage. Individuals recently molted were those that had new
pelage completely covering the dorsal torso. Individuals classified a s between
molts had old pelage covering the entire dorsal torso.
Data on molt state were recorded from 820 examinations, 464 samples of males
(144 individuals) and 358 samples of females (123 individuals). One samplehndividualkalendar month was randomly selected for analysis for individuals examined more than oncekalendar month. This study was part of ongoing research
described elsewhere [Kleiman et al., 1986; Baker et al., 1993; Dietz & Baker,
19931.
RESULTS
A Description of Pelage and Molt in L. rosalia
Although adults were predominantly golden in color, most individuals had
some black fur on ear tufts, wrists, forearms, and/or feet. Variable dappling of the
tail was also common. Some adults retained the black, medial frontoparietal stripe
Molt in Tamarins / 279
characteristic of younger animals [Hershkovitz, 19771. Two observations suggested
geographic variation in pelage coloration among populations. One tamarin captured in the municipality of Saquarema, Rio de Janeiro, 50 km southwest of the
Poco das Antas Reserve, was a darker shade of gold and had more black pelage
than any tamarins observed in the Reserve. Her offspring born in Poco das Antas
Reserve were of similar dark coloration. Six tamarins captured in the municipality
of Cab0 Frio, 42 km southeast of the Reserve, were white-gold in color, a lighter
shade than any individuals observed in POGO
das Antas.
We noted no qualitative sex difference in pelage color, texture, distribution, or
density in the study population. However, we documented three age-specific pelage
types. The pelage of infant tamarins, less than about 10 weeks of age, was golden
in color, lustrous, silky in texture, and sparsely distributed over the body. The
pelage of juveniles older than about 10 weeks of age was straw-colored, relatively
lackluster, of a woolly texture, and densely distributed relative to that of infants.
Adult pelage ranged in color from brown-red to light gold. Underfur, the short,
numerous hairs found beneath the longer guard hairs of many mammals from
temperate regions, was absent at all ages in golden lion tamarins.
We noted partial loss of hair on the tails of a few individuals. In two cases this
condition affected several individuals in the same family group, suggesting a n
ectoparasitic etiology. Parasites found on the pelage of tamarins in Poco das Antas
have been described elsewhere [Goff et al., 1986; Wilson et al., 19891.
New pelage of adults was shiny and golden in color and appeared shorter and
finer than old pelage. Old pelage lacked luster, was usually gold-orange in color,
and was often tipped with a black secretion andlor dirt. Dorsal molt began at the
base of the tail and proceeded cranially along the body and caudally along the tail,
appearing as a longitudinal band of new pelage extending from side to side (Fig. 1).
The point sampling nature of our methods did not allow direct measurement of the
duration of individual molt. However, two males each trapped successively in a
single molting season completed their molt within 5 and 6 weeks. One of these was
classified as between molts on 15 January 1987 and a s recently molted on 6 March
1987. The other was classified as between molts on 11 February 1989 and as
recently molted on 16 March 1989. Also, nearly all tamarins in the study population were individually marked with permanent, black fur dye (nyanzol D; Bellmar,
Inc., North Andover, Mass.) and systematically observed a t intervals of 1week or
less. In all marked individuals, dye marks appeared to fade a t the onset of pelage
molt and disappeared entirely upon completion of molt. Our subjective impression,
based on the fading of these dye marks, is that 5-6 weeks is a reasonable estimate
of the duration of individual molt.
Ten females and 13 males (i.e., 10% of adult samples) were recorded a s in molt
twice during a 12 month period. The mean time between occurrences of first and
second molt for these individuals was 6.08 months (SD = 0.72). The relative
frequencies for calendar months in which either first or second molt was observed
are in parentheses: January (0.141, February (0.071, March (0.02), July (0.121,
August (0.03),September (0.06), and October (0.07).
Population Trends and Correlates of Molt
We determined gross seasonal molt patterns for the study population by calculating the mean percent of samples classified as in molt for each calendar month
(Fig. 2). Although dorsal molt was observed in a few animals in August, 41% of
study samples were in molt in October, the first month of the wet season [Dietz et
al., 19941. The percent of tamarins in molt reached a plateau in excess of 60% from
November-February and declined to levels below 10% by June, the first month of
280 / Dietz et al.
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JUNESEPTEMBER
OCTOBER
DECEMBER
FEBRUARY
Fig. 1. Representative molt patterns for adult golden lion tamarins in the POGO
das Antas Reserve. Old and new
pelage are depieted by light and dark stippling, respectively. After Coimbra-Filho and Maia [19791.
the dry season. The proportion of captures for which tamarins were in molt was
greater during the wet season than during the dry season (wet season: 263 samples
in molt, 188 not in molt; dry season: 10 samples in molt, 239 not in molt; x2 =
196.546, P < 0.001). We found significant positive correlations between mean
monthly percent of samples in molt and precipitation (Pearson correlation coefficient = 0.703, P = 0.011) and minimum daily temperature (Pearson correlation
coefficient = 0.857, P < 0.001) but not the number of births per month in the study
population (Pearson correlation coefficient = 0.368, P = 0.240).
We found no sex differences in the proportion of samples in molt during the wet
season (males vs. all females: x2 = 0.364, P = 0.547; males vs. gravid females: x2
= 0.376, P = 0.540; males vs. nongravid females: x2 = 0.179, P = 0.672) or the dry
season (males vs. all females: x2 = 0.003, P = 0.956; males vs. gravid females: x2
= 0.138, P = 0.710; males vs. nongravid females: x2 = 0.001, P = 0.975). However, when observations from both seasons were combined, the relative frequency
of samples in molt was significantly greater for nongravid females than gravid
females (x2 = 20.843, P < 0.001). The number of samples classified as between
molts and recently molted was, respectively, 87 and 35 for gravid females and 282
and 241 for nongravid females (x2 = 7.631, P = 0.006).
Approximately 10% of our study groups contained two reproductive females,
usually a mother and her daughter. In all but one of these polygynous groups the
older female was socially dominant to the younger [Dietz & Baker, 19931. In all
four cases for which we had data on timing of molt for both females, the dominant
female reproduced first and the subordinate female completed molt first. In three
of these cases the older female was dominant to the younger, and in one case the
younger female was dominant to the older female.
Molt in Tamarins / 281
450
25
400
TENPERATIRE
H
350
%AOLCTSINMOLT
20
300
15
250
200
10
150
100
5
50
0
0
J
F
M
A
M
J
J
A
S
O
N
D
Fig. 2. Relative frequencies of sampled adults in dorsal molt for each calendar month. Data on monthly
precipitation and minimum temperature in the Poco das Antas Reserve after Dietz et al. [19941.
DISCUSSION
Patterns of pelage coloration we describe for L. rosalia in POGO
das Antas do not
differ significantly from accounts by other authors [summarized in Hershkovitz,
19771. However, our observation that L. rosalia from different geographic regions
have distinct and possibly heritable color patterns suggests that genetic drift may
be operating on pelage color of populations in isolated forest fragments.
In contrast with a report by Hershkovitz [19771 stating that callitrichids (except Saguinus oedipus geoffroyi) do not demonstrate a molt line, the process of
dorsal pelage molt we observed in the Poco das Antas population is in general
agreement with that described by Coimbra-Filho and Maia [1979]: that is, distinct
boundaries or molt lines separate recently molted pelage from old pelage on torso
and tail. Molt by tamarins in Poco das Antas began at the base of the tail and
proceeded cranially along the body and caudally along the tail. The direction of
molt we report for L. rosalia is also in contrast with that reported for Saguinus 0.
geoffroyi collected in Colombia and Panama, in which molt on the body apparently
proceeded caudally [Hershkovitz, 19771.
Our findings of an October onset of molt in a wild population conform to those
of Coimbra-Filho and Maia [1979], who reported a September commencement of
molt by tamarins captive in the same geographic region. However, most of the
captive tamarins completed molt by February, while a significant proportion of
das Antas did not complete molt until April or May. This
individuals in POGO
difference may be explained by tighter synchrony of molt in captive animals than
in our free-ranging study population, perhaps due to pheromonal control mechanisms occurring between animals in close physical or olfactory contact. Tight synchrony of ovarian cycles has been described for female L. rosalia in close association in captivity [French & Stribley, 19871. Alternatively, molt in captive
282 I Dietz et al.
tamarins might be shorter than that in free-ranging tamarins, perhaps as a result
of plane of nutrition.
In studies conducted under controlled environmental conditions, day length
has been found to mediate timing of seasonal reproduction in many mammalian
species. However, factors which covary in nature-for example, food availability,
ambient temperature, and precipitation-may also be important cues for onset of
reproduction, thus complicating isolation of the specific environmental cue or cues
triggering seasonal molt in any native population [reviewed in Bronson, 19891.
Molt in the Poco das Antas population commenced in October, roughly midway
between winter and summer solstices in the Southern Hemisphere. The mean date
of fertile copulations for tamarins producing one litterlyear in Poco das Antas was
25 June, 3 days after winter solstice [Dietz et al., 19941, suggesting that the timing
of molt and reproduction is controlled by different environmental cues. The study
of molt patterns of tamarins in zoological parks at various latitudes would be
useful in addressing this question.
Vessey and Morrison [19701 suggested that the onset of molt in two introduced
populations of rhesus monkeys resulted from changes in levels of sex hormones. In
that study the onset of molt took place a t the beginning of the mating season,
whereas tamarins in Poco das Antas began molt a t the beginning of the birth
season. In three of four polygynous groups in the present study, the oldest and
socially dominant female was the first reproductive female to give birth but the
second to complete molt. In one polygynous group the youngest reproductive female was socially dominant, gave birth first, and completed molt first. Although
our sample is small, these data support the hypotheses that social dominance
determines order of birth but age influences the duration of molt in reproductive
females in polygynous groups.
Hypotheses that potentially explain the seasonal timing of molt in the Poco
das Antas population include modification of camouflage patterns appropriate to
predator avoidance, adjustment of pelage insulation appropriate to seasonal
changes in environmental temperature, and timing the energetic expenditure of
protein synthesis of molt to avoid periods of low resource availability or high
energy demand. Our findings do not support the hypothesis that timing of molt is
related to predator evasion. Seasonal changes in pelage coloration were relatively
minor, and, subjectively, we were unable to identify seasonal patterns in predator
density or changes in vegetation patterns that might facilitate predation.
Our observations are consistent with the hypotheses that selective forces mediating timing of molt in Poco das Antas are related to energy conservation. Molt
by most tamarins took place during the warmest months of the year resulting in
fully developed pelage during the coldest months. Similarly, Hershkovitz [ 19771
reported that the majority of specimens of Saguinus 0.oedipus collected during the
rainy season in Colombia were in new or slightly worn pelage, while nearly all
individuals taken in the dry season were between molts. Molt in Poco das Antas
rarely took place during the months of January through August, when food resources were relatively scarce.
Finally, gestation appeared to postpone the onset of molt in reproductive females in L. rosalia in captivity [Coimbra-Filho & Maia, 19791 and Poco das Antas
and in Macaca mulata studied by Vessey and Morrison [1970]. Dietz et al. [1994]
found that birth, lactation, and weaning in L. rosalia in Poco das Antas took place
exclusively during the 7 month wet season, months of maximum food availability
and warmest temperatures, suggesting that timing of reproduction in L. rosalia
has been shaped by energetic cmstraints imposed during the dry season. Timing of
molt may be part of that energy conservation strategy. The occurrence of two molts
Molt in Tamarins / 283
in a 12 month period by 10% of sampled adults, with the second occurring during
the dry season or early wet season, suggests that other selective factors may also
shape timing of molt in this population.
CONCLUSIONS
1. Dorsal molt in wild adult golden lion tamarins began a t the base of the tail
and proceeded cranially and caudally, resulting in two distinct dorsal molt lines.
2. Dorsal molt in this population was seasonal, with greatest frequency from
November-February, months of relatively warm temperatures and abundant food
resources.
3. Most adults underwent dorsal molt once per year. Duration of molt was
estimated at 5-6 weeks. We recorded two molts per season for 10% of sampled
individuals.
4. We found no sex difference in the timing of molt. Pregnancy appeared to
retard the onset and termination of molt.
ACKNOWLEDGMENTS
We thank six Brazilian research assistants for help in capture and examination of study animals and J. Ballou and I. Castro for assistance in data analysis. We
are grateful to M.E. Pereira and three anonymous reviewers for comments on
earlier drafts of this manuscript. The Golden Lion Tamarin Conservation Project
of the Smithsonian Institution provided logistic support. A graduate fellowship
from the National Science Foundation (NSF) and predoctoral fellowship from the
Smithsonian Institution to A. Baker, NSF grants BNS-8616480 and 8941939 to J.
Dietz and BNS-9008161 to J. Dietz and A. Baker, and a n NSF undergraduate
research award to T. Allendorf supported data collection and analysis. Additional
funding was provided by the Smithsonian Institution’s International Environmental Studies Program, National Geographic Society, World Wildlife Fund, and
Friends of the National Zoo. We extend our thanks to D. Pessamilio and other
employees of the Brazilian Institute for the Environment (IBAMA) and to D. Kleiman and A. Coimbra-Filho for their continued support of our research in POGO
das
Antas Reserve.
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