Growing Up Tamarin: Morphology, Reproduction, and Population Demography of Sympatric Free-ranging Saguinus fuscicollis and S. imperator
Date of Award
Doctor of Philosophy (PhD)
Chair and Committee
David T Rasmussen
The Callitrichidae are family of small New World primates with a suite of distinctive morphological and behavioral adaptations that set them apart from other primates. Of primary interest is their reproductive system that includes compulsive twinning: ≥80% of births) and cooperative care of offspring by individuals other than biological parents: termed alloparenting). Further, hematopoietic tissues in callitrichids display signals of both self and sibling DNA, due to an exchange of stem cells early in gestation that renders twin callitrichids as cellular mosaics of each other. This phenomenon is known as genetic chimerism, which increases genetic relatedness between individuals and is likely maintained by cooperative breeding systems. The Callitrichidae are thought to be phyletic dwarfs that exhibit habitual twinning as a derived feature, and accompanied by their tolerance for genetic chimerism, are an important clade to study the evolution of primate reproductive system that has adapted to increased reproductive outputs. They are suspected to be highly polyandrous, where additional male mates assist in the care of a dominant female's reproduction, and subdominant females are reproductively suppressed so that all efforts at alloparenting are directed towards offsetting the high energetic costs of raising a single set of infants of the dominant female. To better understand the evolutionary advantages of this system of reproduction, it is important to document group structure and membership, as well as individual dispersal, reproductive success, and the development of offspring across callitrichid species.
The goal of the present study was to examine group structure, reproductive success and individual growth and development to assess two sympatric Saguinus spp. These data are evaluated in light of the reproductive system proposed for these callitrichids - strict polyandry, cooperative breeding, reproductive suppression, and single reproducing females - in the context of future genetic studies. As such, I attempted to achieve three specific goals - first, an examination of morphological variation between two sympatric callitrichid species; second, an evaluation of age and reproductive status per individual; and third, a comparison of group compositions, mating systems and dispersal patterns of both species to the expected callitrichid reproductive pattern.
I monitored two sympatric species of callitrichids in southeastern Perú at a field site named CICRA over the course of three years - 57 animals in 7 groups of saddleback tamarins: Saguinus fuscicollis), and 36 animals in 6 groups of emperor tamarins: S. imperator). I used an annual capture and release protocol to individually identify all animals, and recorded 19 measures of morphology and dental condition for all subjects. Behavioral data on mating, dispersal, and monthly group-compositions were also obtained, with an emphasis on one focal group per species. I used dental morphology to estimate age for animals ≤ 1 y old: via dental eruption timings) and assigned age-categories for animals ≥ 1 y old via molar occlusal wear. I assessed changes in morphology with age and sex for both species, comparing these measures using Mann-Whitney U tests: α = 0.05), and used reproductive morphology to assign breeding status to adults, identifying primary, secondary, and non-breeders for both sexes. I then identified the predominant mating systems based on the number and sex of breeding adults in a group for both species.
I present here a modified trapping protocol for capturing callitrichids with a dual-step anesthetization protocol that increases animal safety and preserves habituation, resulting in 100% recapture rates. Age-structures predicted by dental wear did not differ significantly between species, or between the sexes for each species. Further sampling of younger adults in the study population is required to conduct population viability analyses. Adult Saguinus imperator: 533 ± SD 79 g females vs. 495 ± SD 45 g males) are significantly heavier than adult S. fuscicollis: 395 ± SD 30 g females vs. 385 ± SD 35 g males), with and without pooled sexes. Among S. imperator, significantly thicker limbs and not an overall increase in body size account for this increased weight. No sexual dimorphism was recorded for either species, save in upper arm lengths among S. fuscicollis: slightly longer in females) and waist circumferences in S. imperator: slightly larger in females, but unrelated to pregnancy).
There are no significant differences between the species in the size of their genitalia or scent glands, despite differing markedly in their physical appearance: i.e shape and pigmentation). No significant effect of month was found on testicular volume, vulvar indices or suprapubic gland areas: Kruskal-Wallis rank sum test, p ≥ 0.05). Suprapubic scent gland areas are significantly higher among females than males for both species: e.g. in S. fuscicollis, gland area =267.5 ± 143 mm for females and 117.1 ± 72.4 mm for males). Vulvar indices explain ca. 70% of variation in suprapubic gland area for females of both S. fuscicollis: R2 = 0.70, P ≤ 0.001) and S. imperator: R2 = 0.76, P ≤ 0.001), while testicular volumes explain suprapubic gland areas only among male S. fuscicollis: R2 = 0.63, P ≤ 0.001). Male S. imperator have undifferentiated glands in general, unrelated to age or breeding status. While vulvar indices initially appear to grow faster than testicular volumes in both species, by 1.5 years of age, males have fully developed genitalia while females still appear underdeveloped. Morphological scores assigned to genitalia and glands encompass their range of variation, and can be used to distinguish infants from adults, but not other age classes: scores are too variable among adults). This highlights the singular importance of evaluating age based on dentition and not reproductive measures for either species, as reproductive suppression can be misleading and cause animals to appear younger than they actually are.
Twinning and strong birth seasonality were observed in both species, with overlapping birth peaks influenced by the environment occurring during the wet season: ca. September to March). Primary breeding males had higher testicular volumes than secondary breeding males: 44-287% higher in S. fuscicollis and 24-80% higher in S. imperator), indicating possible subtle reproductive suppression of males. Secondary breeding females had lower vulvar indices and suprapubic scent gland areas than primary breeding females, and required 2-3 y to acquire secondary breeding status compared to 1 y for males. This is evidence of reproductive suppression of females, but it was not as strict as expected, as evidenced by multiple instances of two primary breeding females reproducing in the same group. Groups of both species display group compositions that encompass multiple adults of both sexes. Their mating systems, however, tend to be polyandrous among S. imperator and polygynandrous among S. fuscicollis. Overall, no sex ratio biases were observed at the level of the population or group; although operational sex ratios indicate that male S. imperator have to share their mate with more males than do male S. fuscicollis.
Immigration events are significantly less common than emigration events, with breeding females having extended tenures in both species. Cold fronts known as friajes create breeding vacancies among groups, which were filled by individuals from outside the group. Overall, Saguinus imperator appears to be more similar in terms infant survivorship and mean reproductive output to both the CICRA and Cocha Cashu populations of S. fuscicollis, than it is to S. mystax at other long-term study sites. However, S. fuscicollis has a slightly higher reproductive output likely achieved by its polygynandrous mating system, maintained by reduced reproductive suppression, in which multiple females breed successfully in a group. Therefore, it does not appear that groups of these two species conform to one, invariable mating system or group structure. It is likely that this variability may apply to other callitrichid species as well. There appear to be more ways than one to be a successful callitrichid. Further years of study, including an investigation of endocrine profiles, genetic population structure, feeding ecology, parasitism and genetic chimerism are also underway at this site, and will lend further insight into the range of variation among callitrichid reproductive systems in the wild.
Watsa, Mrinalini, "Growing Up Tamarin: Morphology, Reproduction, and Population Demography of Sympatric Free-ranging Saguinus fuscicollis and S. imperator" (2013). All Theses and Dissertations (ETDs). 1046.
Permanent URL: http://dx.doi.org/10.7936/K7DB7ZTD