Tamarine – die etwas anderen Primaten

Tamarins – the slightly different primates Unusual for primates, callitrichids are characterized in their social organization by a male‐biased sex ratio and in their social breeding system by a high degree of flexibility with prevailing polyandry, particularly in tamarins. Social polyandry contrasts with a general monopolization of paternities by a single male, i.e. genetic monogamy. Unique amongst primates (and very rare amongst mammals in general) is the cooperative breeding, where apart from fathers other group members, particularly adult males, participate in the transport of infants, generally twins. Finally, female tamarins show much higher rates of scent marking and possess much larger scent glands than males. In combination with the chemical composition of scent marks, this is most plausibly interpreted as a “quality indicator” in the sense of sexual selection theory.     

A comparative perspective on the evolution of tamarin and marmoset social systems

Tamarins and marmosets (callitrichids) present an unusual opportunity for study of the determinants of primate social systems, because both the mating and infant care patterns of callitrichids are variable, even within individual populations. In this paper, I briefly describe three characteristics of callitrichid social systems that distinguish them from most other primates: extensive male parental care, helping by nonreproductive individuals, and variable mating patterns. I then discuss the evolution of these characteristics and of the frequent twinning exhibited by callitrichids. I suggest that an ancestor of modern callitrichids gave birth to a single offspring at a time, mated monogamously, and had significant paternal care. The idea that males of this ancestral form must have provided paternal care, even though only single infants were born, derives from a comparison of litter/mother weight ratios in modern primate species. Twinning perhaps then evolved because of a combination of dwarfing in the callitrichid lineage, leading to higher litter/mother weight ratios, and a high infant mortality rate, and because the extensive paternal care already present facilitated the raising of twins. I propose that the helping behavior of older offspring may have coevolved with twinning, because helpers would have increased the chances of survival of twins, and the presence of twins would have increased the benefits of helping. Finally, the high costs of raising twins and the variability of group compositions, especially the fact that some groups would not have had older offspring to serve as helpers, may have selected for facultative polyandry in saddle-back tamarins (Saguinus fuscicollis) and perhaps in other callitrichid species. Both helping and cooperative polyandry have been extensively studied in bird species, and I apply some of the conclusions of these studies to the discussion of the evolution of callitrichid social systems.     

THE CHARACTERISTICS AND OCCURRENCE OF COOPERATIVE POLYANDRY

This paper discusses the relative position of cooperative polyandry among models for the evolution of both polyandry and cooperative breeding. Cooperative polyandry is described as the situation where more than one male and one female breed as a group with males sharing equally in copulations and the care of one set of young. Sequential and simultaneous polyandry are defined to show how they differ from cooperative polyandry. These systems generally are characterized by the care of only one parent for each set of young, a trait which is in sharp contrast to cooperative polyandry. An argument is made that the present models for the evolution of polyandry cannot be expanded to include the cooperatively polyandrous species. Instead, the cooperative traits of cooperative polyandry fit within the array of characteristics of cooperative (communal) breeding. General characteristics of all cooperative species (monogamous, promiscuous and polyandrous) are reviewed and possible reasons for the evolution of equal-status males are discussed. A plea is made for the unification of evolutionary models dealing with mating systems and cooperative systems.     

Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus)

We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the apparatus for access to rewards. Resistance was applied to both handles so that two tamarins had to act simultaneously in order to receive rewards. In contrast to several previous studies of cooperation, both tamarins received rewards as a result of simultaneous pulling. The results from two experiments indicated that the cottontop tamarins (1) had a much higher success rate and efficiency of pulling than many of the other species previously studied, (2) adjusted pulling behaviour to the presence or absence of a partner, and (3) spontaneously developed sustained pulling techniques to solve the task. These findings suggest that cottontop tamarins understand the role of the partner in this cooperative task, a cognitive ability widely ascribed only to great apes. The cooperative social system of tamarins, the intuitive design of the apparatus, and the provision of rewards to both participants may explain the performance of the tamarins.     

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males—those who joined the group after infants were conceived—participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.     

Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: Evidence from a thirteen-year study of a marked population

We monitored a population of four to seven groups of individually marked saddle-back tamarins (Saguinus fuscicollis; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park every year from 1979 through 1992. In this paper we use data on life histories, group compositions, group formations, and dispersal patterns collected during these 13 years to examine the reproductive strategies of males and females. Group compositions and mating patterns were quite variable in this population, with both monogamy and cooperative polyandry common. In polyandrous groups, two males shared a female's copulations and cooperatively cared for her young. Although most groups contained a single breeding female, we recorded four cases in which secondary females successfully reared young. Most young females appeared to wait in their natal groups for the first opportunity to fill a primary breeding position in their own or a neighboring group. Females that acquired primary breeding positions maintained those positions for a mean of 3 years. No female was observed to transfer between groups a second time. Variation in female lifetime reproductive success was high. Half of the females marked as juveniles never bred; the other half produced an average of 3.5 young. A paucity of female breeding opportunities may explain the high mortality of females between 2.5 and 4.5 years of age and the resulting male-biased adult sex ratio. The majority of groups contained more than one probable male breeder. Polyandrous groups included both related and unrelated males. Behavioral differences between Cocha Cashu tamarins and other studied populations may result from the pressures of living in an environment inhabited by nine other primate species and numerous predators. © 1996 Wiley-Liss, Inc.     

High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia)

Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.     

Varying Ecological Quality Influences the Probability of Polyandry in White-handed Gibbons (Hylobates lar) in Thailand

Although members of the family Hylobatidae are known to be monogamous, adult white-handed gibbons ( Hylobates lar ) at Khao Yai National Park, Thailand, also show multimale groups and polyandry. A need for more than one male to successfully raise offspring cannot explain the occurrence of polyandry in these territorial primates, because direct paternal care is absent in this species. We hypothesize that polyandry is primarily related to costs/benefits for males of cooperatively defending a female and/or resources; our prediction was that polyandry would become more frequent with increasing costs of female/resource defense. We measured the ecological quality of seven gibbon home ranges over a 3-yr period (2001–2003) to investigate how resource availability affected the probability of polyandry, and found a significant negative relationship between home range quality and home range size. Larger home ranges were of lower quality. As predicted, groups living on larger, poorer home ranges also experienced longer periods of polyandry. In forest areas of comparatively low quality, acquiring and maintaining a large home range that includes enough resources for a female to reproduce steadily may surpass a single male's capacity. Our model of cooperative male polyandry was supported by preliminary data of shared territorial defense and access to the female. However, interaction proportions were strongly skewed, and female's primary male partners monopolized grooming and mating. Nevertheless, a primary male on a large territory may benefit from the presence of a secondary male with aid in territorial/female defense, whereas a secondary male may gain by avoiding high dispersal costs.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Evolution of polyandry in a communal breeding system

The evolution of polyandry requires an asymmetrical factor thatfavors more matings per breeding female than per breeding male,thus reversing Bateman's principle. Here a model is presentedfor the evolution of avian cooperative polyandry. The modelshows that polyandry can evolve if communal breeding is initiallyadvantageous and if increasing clutch size beyond an optimumis detrimental. The advantage of communal breeding favors theaddition of more breeders (either males or females) and thusselects against breeding as single pairs (monogamy). The optimaldutch size creates the asymmetry that favors adding male breeders(polyandry) over adding female breeders (polygyny). Adding femalesis detrimental because females must lay eggs to reproduce andcan therefore increase the clutch size of the group. On theother hand, males can reproduce by sharing paternity withoutincreasing dutch size. It is shown that cooperative polyandryevolves either because it maximizes both male and female fitnessor because polygyny and monogamy are behaviorally unstable.Data from acorn woodpeckers support the assumptions of the modeland suggest that cooperative polyandry evolved because it isbehaviorally more stable. The persistence of monogamy and polygynyin acorn woodpeckers (at a lower incidence than polyandry) isalso examined. Polygyny in these birds represents a case ofthe Prisoner's Dilemma     

The Effect of Infant Body Mass on Carrier Travel Speed in Cotton-top Tamarins (Saguinus oedipus)

Infant carrying is common in primates and may be the second most costly activity related to reproduction, after lactation. In cooperative breeding groups of callitrichids, all group members carry and care for twin infants. Previous studies have described the costs of infant carrying in terms of body mass loss and reduced locomotor capability. However, infant carrying may also influence travel speed, an important potential cost because slower speed may handicap foraging, energetic budgets, and predator avoidance. We evaluated the impact of infant carrying on the travel speed of 27 adult and 9 subadult cotton-top tamarins (Saguinus oedipus) of both sexes in large outdoor enclosures. We compared carrier speed to speed when not carrying during the 10 weeks after nine births. Subadult tamarins, which have a lower body mass than adults do, moved faster than adults when not carrying. We found no difference between the mean speeds of subadults and adults while carrying. However, the speed of carriers decreased as infant mass increased, and the slope of this negative relationship was more pronounced in subadult carriers. For every 80 g of extra mass load (the body mass of newborn twins), adults reduced their speed by 6 % and subadults by 19 % relative to noncarrying speed. We also observed a reduction in speed while carrying two infants in adult tamarins as carrying time increased. Our results contribute to an understanding of the costs of infant carrying, and serve to emphasize the importance of cooperative breeding systems in coping with these costs.     

No selection for change in polyandry under experimental evolution

What drives mating system variation is a major question in evolutionary biology. Female multiple mating (polyandry) has diverse evolutionary consequences, and there are many potential benefits and costs of polyandry. However, our understanding of its evolution is biased towards studies enforcing monandry in polyandrous species. What drives and maintains variation in polyandry between individuals, genotypes, populations and species remains poorly understood. Genetic variation in polyandry may be actively maintained by selection, or arise by chance if polyandry is selectively neutral. In Drosophila pseudoobscura, there is genetic variation in polyandry between and within populations. We used isofemale lines to found replicate populations with high or low initial levels of polyandry and tracked polyandry under experimental evolution over seven generations. Polyandry remained relatively stable, reflecting the starting frequencies of the experimental populations. There were no clear fitness differences between high versus low polyandry genotypes, and there was no signature of balancing selection. We confirmed these patterns in direct comparisons between evolved and ancestral females and found no consequences of polyandry for female fecundity. The absence of differential selection even when initiating populations with major differences in polyandry casts some doubt on the importance of polyandry for female fitness.     

Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus), and its relationship to infant care

Male cotton-top tamarins have been shown to be responsive to female scent cues of ovulation, and are known to actively participate in infant care during the time when their mates are fertile. We measured urinary androgen levels and glucocorticoids in seven father tamarins for the first month following the birth of infants to determine 1) whether male tamarins showed an androgen response to their mate's postpartum ovulation, 2) when androgens rise relative to ovulation, 3) whether there is a glucocorticoid response, and 4) whether males alter their parenting behavior during their mate's receptive period. All of the males showed a significant increase in urinary androgens prior to the female's postpartum LH peak, which indicated ovulation. The hormonal increase, which included estradiol, occurred 3-7 days prior to the female's LH peak at a time that coincided with the female's follicular period. Corticosterone levels also peaked during that time, but did not correlate with androgen changes. Fathers did not alter their daily infant-carrying patterns relative to the androgen increase or at the time of the mate's LH peak. We conclude that male cotton-top tamarins experience an increase in androgens that coincides with their mate's postpartum ovulation, which ensures optimal fertility. However, this sexual communication does not alter father-infant interactions, which already occur at a high rate in this species.     

Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints

Sleeping sites are an important aspect of an animal's ecology given the length of time that they spend in them. The sleep ecology of wild saddleback and mustached tamarins is examined using a long-term data set covering three mixed-species troops and 1,300+ tamarin nights. Seasonal changes in photoperiod accounted for a significant amount of variation in sleeping site entry and exit times. Time of exit was more closely correlated with sunrise than time of entry was with sunset. Both species entered their sleeping sites when light levels were significantly higher than when they left them in the morning. Troops of both species used >80 individual sites, the majority being used once. Mustached tamarins never used the same site for more than two consecutive nights, but saddlebacks reused the same site for up to four consecutive nights. Mustached tamarins slept at significantly greater heights than saddleback tamarins. There were consistent interspecific differences in the types of sites used. Neither the presence of infants, season, nor rainfall affected the types or heights of sites chosen. Sleeping sites were located in the central area of exclusive use more often than expected, and their position with respect to fruiting trees indicated a strategy closer to that of a multiple central place forager than a central place forager. These findings are discussed in light of species ecology, with particular reference to predation risk, which is indicated as the major factor influencing the pattern of sleeping site use in these species.     

Food sharing in lion tamarins: Tests of three hypotheses

Infant marmosets and tamarins (Callitrichidae) frequently receive food from older group members. Three possible functions of food sharing in lion tamarins were examined experimentally. The first hypothesis, that food sharing ensures that infants receive sufficient food even if it is difficult for them to acquire it themselves, was tested by varying the ease with which infants could reach a food source. When access to food was restricted, infants fed themselves less, received more food from others, and had a higher success rate in begging attempts. The second hypothesis, that food sharing helps teach infants an appropriate diet, was tested by presenting fruits that were novel to infants. Although infants fed themselves less under these conditions, adults were less likely to share novel foods than familiar foods. The final experiment compared food sharing when food was abundant with behavior when food items were presented singly. Infants fed themselves less and received more food from others when food items were rare. These results suggest that food sharing in lion tamarins helps to ensure that infants receive adequate amounts of food which is difficult to locate or acquire, but that it is not involved in teaching infants which foods they should eat. © 1993 Wiley-Liss, Inc.     

Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru

Kaytydids and related insects are an important component in the diets of moustached ( Saguinus mystax mystax ) and saddle-back tamarins ( Saguinus fuscicollis nigrifrons ). Based on preliminary data of captured prey, trends suggest that partitioning occurs regarding orthopterans as a limited food resource. Of species caputre as prey, only three were shared by both tamarin species. Saddle-back tamarins appeared to specialize more on understorey species (0-4 m), concentrating on pseudophylline katydids. Moustached tamarins incorporated a greater percentage of phaneropterine katydids from the lower to middle canopy into their diet of insects. Although most prey species were exposed to view during the diurnal feeding period of the tamarins, only the saddle-back tamarin fed on katydids that spend the day concealed from view within dead curled leaves. Differentiation of the prey spectrum may represent a critical pattern of niche differentiation in these two sympatric tamarin species, which show a high overlap in their plant food resources.     

Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia)

Background Wild golden lion tamarins from the Biological Reserve of Poço das Antas, Rio de Janeiro, Brazil, have high prevalence of Trypanosoma cruzi infection leading us to clinically assess the disease in this endangered species. Methods 34 tamarins were sampled for the presence of T. cruzi infection (through serology) and clinical evaluation (electrocardiography, blood counts and biochemical analysis). Results 32% of the sampled tamarins were T. cruzi positive, 45% of these displayed cardiac abnormalities. Main cardiac abnormality in infected tamarins was T wave low voltage; R wave low voltage and V3S wave high voltage were also found. The tamarins displaying T wave low voltage had high proportion of seric cardiac creatine kinase. Seric mean total protein was significantly higher in infected tamarins. Conclusions Sampled tamarins displayed typical signs of T. cruzi infection, similar to experimentally infected primates and human natural infection. Potential risk of T. cruzi infection to this endangered species is discussed.     

Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): interactions with gender, androgen levels, and parenting

Unlike biparental bird and rodent species, mating and parenting occur simultaneously in cotton-top tamarins, Saguinus oedipus, providing a unique model for examining endocrine interactions. This study was designed to determine the relationship of prolactin to testicular androgens during parenting and mating. Specifically we examined (1) the patterns of postpartum prolactin excretion in male and female tamarins with and without infant survival; (2) the relationship between androgen and prolactin levels during the periparturitional period in male tamarins; and (3) male hormonal response to the postpartum mating that occurs simultaneously with paternal care. All females showed an elevation in prolactin during the first week postpartum and when infants died, female prolactin levels decreased significantly. Infant survival during the first 15 days did not influence male levels of prolactin, cortisol, or the testicular androgens testosterone and dihydrotestosterone (DHT). Prolactin did not show an inverse relationship with any of the androgens (testosterone, DHT) studied during the postpartum period. No significant differences in hormones were found between prepartum levels and the first, second, and third 5-day blocks postpartum for all 10 males. Males who had infant-care experience showed an increase in testosterone during the first 5 days postpartum and prolactin levels correlated with the number of previous births a male had experienced. However, the most significant changes in testosterone occurred in males whose mates ovulated during the first 15 days following birth in contrast to males whose mates ovulated later than 15 days. These results indicate that unlike females, male tamarins are not showing hormonal changes in response to infants. Urinary androgens did not show an inverse relationship to prolactin in male tamarins, but were elevated concurrent with the female's fertile period.     

Seasonal Variation in Seed Dispersal by Tamarins Alters Seed Rain in a Secondary Rain Forest

Reduced dispersal of large seeds into degraded areas is one of the major factors limiting rain forest regeneration, as many seed dispersers capable of transporting large seeds avoid these sites with a limited forest cover. However, the small size of tamarins allows them to use small trees, and hence to disperse seeds into young secondary forests. Seasonal variations in diet and home range use might modify their contribution to forest regeneration through an impact on the seed rain. For a 2-yr period, we followed a mixed-species group of tamarins in Peru to determine how their role as seed dispersers in a 9-yr-old secondary-growth forest varied across seasons. These tamarins dispersed small to large seeds of 166 tree species, 63 of which were into a degraded area. Tamarins’ efficiency in dispersing seeds from primary to secondary forest varied across seasons. During the late wet season, high dietary diversity and long forays in secondary forest allowed them to disperse large seeds involved in later stages of regeneration. This occurred precisely when tamarins spent a more equal amount of time eating a high diversity of fruit species in primary forest and pioneer species in secondary forest. We hypothesized that well-balanced fruit availability induced the movement of seed dispersers between these 2 habitats. The noteworthy number of large-seeded plant species dispersed by such small primates suggests that tamarins play an important, but previously neglected, role in the regeneration and maintenance of forest structure.     

Effects of allocare-givers on fitness of infants and parents in callitrichid primates

The effects of callitrichid primate helpers (allocare-givers other than an infant's father) on the survival, reproduction or behavior of infants and parents are reviewed, using both published studies and data from free-ranging golden lion tamarins (Leontopithecus rosalia). Three lines of evidence suggest that helpers may increase their own inclusive fitness: (1) The number of adult males acting as helpers in free-ranging groups is correlated with the number of surviving infants in 3 callitrichid species. However, the lack of a negative correlation with number of infants dying suggests that activities other than direct infant care (e.g. territory defense) may be more important, especially in newly formed groups. (2) In 2 species, captive groups with helpers carry infants for longer periods of time than do groups without helpers. Whether such differences would translate into meaningful survival differences in free-ranging groups is unclear. (3) Helpers reduce the energetic burden of parents by reducing the amount of time they spend transporting or provisioning infants in at least 4 species. Reproductive males are more likely than reproductive females to benefit from the presence of helpers, reducing their investment in infant care activities as the number of helpers in the group increases. In free-ranging golden lion tamarins, the reproductive tenure of males, but not females, increases with the number of helpers in the group, suggesting that a reduction in energetic investment may translate into increased survival. 'Decisions' made by helpers to participate in infant transport are weighed against competing needs for foraging, vigilance, territory defense and, in some cases, prospecting for breeding opportunities. Given this complexity, a sophisticated model may be required to answer the question of how helpers 'decide' to participate in infant care versus other activities.