Proyecto Titi has been actively involved in studying wild cotton-top tamarins for many years at our field sites in Colosó and Santa Catalina. We present a short overview of some of our publications on the behavior, reproductive patterns, and parental care strategies of this fascinating primate. As habitat for cotton-tops continues to be threatened in Colombia, it is essential that we document how this will effect this critically endangered primate for the future. We will continue to post information on our publications as they become available.
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Savage, A., Soto, L., Lamilla, I. and Guillen, R. 2009. Cotton-top tamarin Saguinus oedipus (Linnaeus, 1758). In: R. A. Mittermeier et al., Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010, pp.68-71. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI), Arlington, VA.
Cotton-top tamarins are Critically Endangered and found only in northwestern Colombia. They have an extremely limited distribution, occurring in northwestern Colombia between the Río Atrato and the lower Río Cauca and Rio Magdalena, in the departments of Atlántico, Sucre, Córdoba, western Bolívar, northwestern and northeastern Chocó east of the Río Atrato. Colombia is among the top ten countries suffering deforestation, losing more than 4,000 km² annually. There are just three protected areas in the historic range of the cotton-top tamarin — Parque Nacional Natural Paramillo (460,000 ha), Santuario de Flora y Fauna Los Colorados (1,000 ha) and Montes de María Reserve (7,460 ha). These protected areas have lost 42%, 71%, and 70% of their forests, respectively, since they were created.
Aside from deforestation, in the late 1960s and early 1970s, 20,000–40,000 cotton-top tamarins were exported to the United States for use in biomedical research. Today, cotton-top tamarins continue to be threatened by capture for the illegal pet trade, despite international laws condemning the activity. A recent population census was conducted in the historic distribution of the species that documented a dramatic decline in suitable habitat, and concluded that fewer than 6,000 cotton-top tamarins remain in the wild.
To aid in the conservation of the cotton-top tamarin, we established Proyecto Tití, a multi-disciplinary, in situ conservation program that combines field research, education initiatives and community development for the conservation of natural resources that is economically feasible for local communities in Colombia.
We developed classroom and field activities for elementary and secondary school children that were designed to create an awareness of the plight of the cotton-top tamarin and engage students in a variety of activities in the classroom and field, and in international exchanges that would promote the conservation of Colombia’s natural resources. We developed a strong partnership with the Barranquilla Zoo, and we now reach urban audiences though a series of classroom workbooks (CARTITILLA) aimed at 5–7th grade school children. It was used in 15 schools with more than 3,000 students. Our evaluations showed an 81% increase in the level of accuracy on correctly identifying a cotton-top tamarin, a 77% increase in understanding that cotton-top tamarins are found only in Colombia, and a 65% increase in the understanding of the pet trade as a threat to the survival of the species.
A family of five used approximately 15 logs a day to cook their food over an open fire. In discussions with local villagers in Colombia we discovered the traditional Colombian “binde”, a small cooking stove that was made from a termite mound would help with this problem. Interviews with local villagers indicated that bindes required less firewood than cooking over an open fire but while accepted by local communities in Colombia, bindes were made from termite mounds and they would quickly crack and disintegrate with repeated use and were consequently little favored. Proyecto Tití designed a durable binde made of clay that was readily accepted by the communities and proved to significantly reduce the amount of firewood consumed. Using a binde, the number of logs consumed each day was reduced by two-thirds.
Efforts to manage waste are also a challenge in local villages, and the situation is worsening, particularly in growing rural communities where disposal is generally by burning or by dumping in rivers or on the roadside. A program was developed to turn the trash into a source of income. The goal was to create an artisan group that would make a product from the numerous plastic bags, so as to provide a stable income that, combined with effective conservation education messaging, would result in a commitment to protect the forests, and reduce the capture of cotton-top tamarins for the illegal pet trade. Proyecto Titi first engaged the village of Los Limites in protecting cotton-top tamarins and their habitat by helping it with the confection of tote bags crocheted with recycled plastic bags called “eco-mochilas.” Fifteen women began the initiative, and were so successful it was necessary to provide business training as they became established entrepreneurs, developing products of a quality that sells in national and international markets.
Proyecto Tití demonstrated a clear economic benefit to individuals that participate in community empowerment programs and produced tangible results that are contributing to the survival of the cotton-top tamarin in Colombia.
Savage A, Giraldo LH, Blumer ES, Soto LH, Snowdon CT. 1996a. Demography, group composition, and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups. American Journal of Primatology 37:23-32.
Tamarins live in social groups of 2-10 individuals. Although, there have been a few cases of reported polygamy, most groups contain only one reproductively active male and female (Neyman 1977). Females, on average, give birth to twins annually. Social groups appear relatively stable, with an average rate of emigration of 0.71 ± 1.18 individuals/group/year. Males and females disperse to neighboring groups equally, however, adults move more frequently than juveniles and infants. Immigrant males are more likely to enter a group following the death of a resident male. Reproductive success of these immigrant males is difficult to quantify without paternity tests, however, an immigrant male may release subordinate females from reproductive suppression. A novel male avoids the constraints of incest avoidance, and may thus stimulate a reproductively inhibited female. If a female immigrates, she does not necessarily assume the breeding position. Emigration increased to 2.8 individuals/group/year during a drought , suggesting movement between groups may be a result of extreme environmental conditions leading to increased competition for limited resources.
A proposed model to illustrate the potential reproductive strategies of cotton-top tamarins:
Savage A, Shideler SE, Soto LH, Causado J, Giraldo LH, Lasley BL, Snowdon CT. 1997. Reproductive events of wild cotton-top tamarins in Colombia. American Journal of Primatology 43: 329-337.
In collaboration with Drs. Bill Lasley and Susan Shideler of the University of California-Davis, we have developed methods for assaying estrone glucuronide (E1C) and progesterone (PdG) in both urine and feces of cotton-top tamarins. We have also successfully developed a technique to collect daily fecal samples from wild tamarins. We are in the process of further examining the factors controlling reproductive events of different populations of wild tamarins. This will allow us to compare the reproductive cycles of both wild and captive tamarins and examine the mechanisms regulating fertility in the wild.
Captive female tamarins have a gestational length of 183 days and an ovulatory cycle of 18 days (Ziegler et al. 1987). Females have an 18-day post-partum estrus and 80% of these ovulations result in conception. In the wild, females have an average 144 day post-partum suppression of fertility, which appears to be influenced by environmental conditions. Assays reflect conception with E1C levels ranging >4,000 ng/g and PdG >8ug/g. Hormone levels drop following parturition (E1C to <1000 ng/g and PdG to <3 ug/g).
Reproductively active females are also capable of influencing the fertility of other females in the group. In both the wild and captivity, post-pubescent females are reproductively suppressed, appearing acyclic, while they remain in their family. In order for a female to become reproductively active, she must be removed from her family and paired with a novel male. Phermones have been implicated as one of the factors mediating this suppression. Captive females removed from their family, paired with a novel male and exposed to scent secretions from their mother, took longer to ovulate than those females in a contol condition. Males also influence a female's fertility. Males can accelerate puberty in prepubescent females. Moreover, pairing a female with a "familiar" male (eg. brother) will not cause the female to become reproductively active. Females will ovulate only in the presence of a novel male.
The cycles of wild daughters were monitored while in their natal group. One female cycled irregularly during her mother's period of postpartum infertility. When her mother conceived again, she was observed to ovulate and conceive herself. Resulting aggression between mother and daughter ended in the eviction of the daughter from the group prior to parturition. The second daughter exhibited normal cycles, however, following the birth of siblings, there was a dramatic decline in hormone levels that remained low through her mother's next conception.
While females in captivity are observed to reproduce twice a year, wild females give birth only once a year, prior to the rainy season. The birth period appears to be correlated with the greatest consumption of fruit and insects in the diet. And diet composition may also influence fecundity, whether a female has a single infant or twins. See the list of plants cotton-tops feed from.
Savage A. Snowdon CT, Giraldo LH. 1996b. Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus). In Adaptive Radiations of Neotropical Primates. Eds. M Norconk, A Rosenberger, P Garber. New York: Plenum Press.
Parental care in this species is shared by all group members. Early infant caretaking experience, observed in captivity, has been found to influence future reproductive success in both males and females. If an animal has never carried an infant on its back while it was in its family it will abuse its own offspring. However, if the animal has experience caring for offspring prior to reproduction, it will successfully care for its offspring. Interestingly, non-natal animals are actively involved in infant care and are often observed assuming sentinel positions in their new groups. An animal never carries infants while involved in "sentry" duty. The sentry remains vigilant while the group forages or rests and is responsible for notifying the group of any potential threats to their safety.
Observations of 12 births in the wild showed that infants are carried exclusively during the first four weeks of development, with a gradual decrease during weeks 5-9, such that by week 10, the infants are solo for nearly 50% of the observation time. All individuals in the group carry the infants, though adults were more likely to than juveniles. There was no significant difference in carrying time between males and females. Primiparous females, however, carry their infants more during their first two weeks, than multiparous females. Infant survival to one year of age increases with group size (see Table 1 below). Contribution of the mother in infant care remains independent of group size, however, the larger the group, the less time the adult males carried infants. The adult male however, exhibits more vigilant behavior and assumes the sentry position more often that the adult female during this time. Adult vigilant behavior also increases as the infant becomes more independent.
Table 1. Infant survival as a function of group size.
A., Soto, L., Medina, F., Emeris, G., & Soltis, J. (2009). Litter Size
and Infant Survivorship in Wild
Developing successful conservation programs for endangered primates requires a complete understanding of the factors involved in successful reproduction and causes of infant mortality. In contrast to other nonhuman primates, callitrichids are unusual as litter size can vary between one to five offspring in captivity. Twins tend to be the norm for most callitrichids, but the incidence of triplet and quadruplet births can account for nearly 10–50% of the litters born in captive colonies. Litter size significantly influences the survivorship of infants with twins having a higher survivorship than triplets or quadruplets. In the wild, reports suggest that twin and singleton litters were the norm in most callitrichids studied to date. Incidence of triplet births is very low in the wild, but there have been triplets observed in a Golden Lion Tamarin family where none of the offspring survived and in a Common Marmoset family where evidence was found of survival.
In our study, there were fifty-eight litters from 21 females recorded at the two field sites. Twins were most common (81%), followed by singletons (16%), and we had the first report of triplet births (3%) in wild cotton-top tamarins. Mortality was not uniformly distributed across time with 33% of cases confined to the first week. Determining the sex of the offspring rarely occurred if infants died or were missing from the group, and carcasses of infants were rarely found. Thus, calculating an accurate sex ratio of infants was not possible. However, surviving offspring were comprised of 42 males and 32 females. Determining the immediate cause of mortality was also challenging. Two of the six carcasses that were recovered were too decomposed to determine the cause of death. The remaining four carcasses were from the two observed triplet births and malnutrition was deemed the cause of death.
Fourteen females produced more than one litter. For these females, the mean survival rate to 6 months for first litters was 57%710.3 SEM but the mean across subsequent litters rose to 86%77.6. However, the effects of parity were not as clear. One primiparous female (Nadia) left her family group and assumed the position of the reproductively active female in a neighboring group and she gave birth to twins that survived to 6 months. However, two primiparous females (Milena and Tamara) were identified in the Santa Catalina sample but do not represent ‘‘typical’’ primiparous females as they were in groups containing two pregnant females. Milena successfully cared for her twins until one was observed missing from the group at week 8 and Tamara’s twins were ‘‘kidnapped’’ by her mother and subsequently died. Litter size appeared to influence survival with triplet litters showing a lower infant survival to 6 months (33%) than twins (80%) or singletons (77%), although the number of triplet litters (n52) is too small for statistical analysis.
This study confirms that infant survival to 6 months of age in the wild (78% twins and 88% singletons), gathered from two distinct field sites, and was greater than has been reported in captive colonies. Similar to captive colonies mortality was highest during the first week of life; however, given the low rate of carcass retrieval we cannot determine the cause of mortality and infant mortality associated after 20 days may be related to the development of infant independence. Given that the parity of the majority of our study females could not be determined, we did find that infant mortality was higher in first litters than subsequent litters born to wild cotton-top tamarin females. We were unable to find a significant relationship between infant mortality and group size or the number of adult males in a social group. However, there was a trend toward higher mortality with a shorter inter-birth interval. The number of females that produce multiple litters in 1 year is rare, but infants born out of the normal birthing season may be at risk as food may not be as plentiful for a nursing female.
Miller, L., Savage, A., Giraldo, H. Quantifying the remaining forested habitat within the historic distribution of the cotton-top tamarin (Saguinus oedipus) in Colombia: Implications for long-term conservation. American Journal of Primatology, 64:451-457, 2004
Landsat Thematic Mapper (TM) data was used to classify forested areas within the historic distribution of cotton-top tamarins (Saguinus oedipus) in Colombia. Cotton-top tamarins are a critically endangered species endemic to the northwest region of Colombia. This critically endangered species faces continued deforestation within its historical distribution in Colombia, thus, it is critical to develop strategies to protect tamarins and their habitat. Between 1990-2000, 31% of the forested habitat within the tamarins’ historic distribution has been lost. Agriculture, urban development, and logging have caused a significant decrease in remaining forested habitat on both private lands and in protected parks and reserves. It is estimated that since the inception of the protected lands (Parque Nacional Natural Paramillo, Santuarío de Fauna y Flora Los Colorados, and Reserva Forestal de Montes de Maria) almost 43% of the forested area within the parks boundaries have been lost. With an annual increase in human population in Colombia of 1.6% [Patel, 2002] it is important to target specific areas for protection while creating mitigation strategies to compensate for economic growth. The results of this study provide valuable information to assist in the long-term development of effective conservation strategies for this critically endangered primate.
Savage, A., Guillen, R., Lamilla, I., & Soto, L. (2010). Developing an
Effective Community Conservation
Developing effective primate conservation programs, which address the conservation needs of the animals and the needs of local communities that directly impact the habitats that the primates need to survive, is a challenging task. Proyecto Tití´ has provided economic alternatives to local communities that have dramatically reduced the illegal capture of cotton-top tamarins and forest destruction in the region that has positively impacted the long-term survival of this critically endangered primate. Although primate conservation programs can indeed focus on creating knowledgeable individuals, issues relating to poverty can override the most well-educated communities, thus putting the long-term conservation of primates and their habitats at continued risk. The trend in successful conservation programs has been one of integrated rural development that demonstrate direct benefit to the local people (money, jobs, access to health related resources, and food) by conserving species and their habitats.
Understanding the root causes of primate population decline is essential in the development of a comprehensive conservation program. Proyecto Titi has focused efforts on (1) long-term monitoring of the reproductive and behavioral biology of the cotton-top tamarin; (2) documenting the loss of forested habitat, developing techniques to accurately estimate the remaining wild population, and monitoring them over time; and (3) identifying factors that contribute to the decline of this critically endangered species.
Long-term monitoring of species
We began by developing field sites within the historic distribution of cotton-top tamarins, so that we could conduct long-term field studies to investigate the reproductive and behavioral biology of this species. Having data from two field sites allowed us to compare a variety of factors (fecundity, survival rates, home range size, feeding ecology, group dynamics, etc.) to determine if there were any biological causes that were influencing the long-term survival of the species. Our studies have shown that wild cotton-top tamarins do not appear to have high rates of adult or infant mortality, issues of disease exposure, or any obvious biological cause for their decline at our study sites. However, we have observed challenges with animals effectively dispersing, given the limited forested habitat in the area.
Documenting forest loss and species decline
Colombia is among the top ten countries to suffer significant loss of forested habitat with a 0.5% annual rate of destruction and the status of their forest habitat has been designated critically endangered throughout a significant portion of Colombia. A study by Miller et al.  documented a 31% decrease in forested habitat within the tamarins’ historic distribution between 1990 and 2000, because of the conversion of tropical forest habitat to agricultural uses and urban development, extraction of forest resources for firewood and lumber, and logging on both private and protected areas.
Given the rapid rate of forest decline, it was imperative to develop a population monitoring program for the cotton-top tamarin. Given their small size, arboreal nature, and fear of humans, using standard line transect sampling methods dramatically underestimates the size of the population. We, therefore, developed a collaboration with scientists from the Centre for Research into Ecological and Environmental Modeling at the University of St. Andrews, and created a ‘‘lure strip transect,’’ which combines the use of playbacks of territorial vocalizations with traditional transect surveys to yield a robust method of estimating population size. The results from our census found a dramatic decline in the existing cotton-top tamarin population in Colombia. Given the marked decline in suitable forest habitat combined with a small population, the cotton-top tamarin has been reclassified as Critically Endangered by the International Union for Conservation of Nature (IUCN) [IUCN, 2008].
Factors influencing the long-term survival of cottontop tamarins
Our studies show that the primary threats to the survival of the cotton-top tamarin has been the dramatic loss of habitat from the conversion of tropical forest habitat to agricultural uses, extraction of forest resources for firewood and lumber, and capture for sale in the illegal pet trade. This destruction and consumption of forest resources is driven by the fact that 65% of the population in Colombia lives below the poverty line. With a lack of sustainable income, limited access to employment opportunities, and lack of knowledge of the long-term impact of continued unsustainable extraction of forest products, the future of cotton-top tamarins and the biodiversity in Colombia is severely threatened.
Our early studies found that there were many myths and misconceptions about the forest and the wildlife of the area. More than 90% of the population we surveyed had no idea that cotton-top tamarins were endemic to Colombia and not found in other countries. Our educational strategy involved developing formal and informal programs that (1) increased awareness to the plight of the cotton-top tamarin and the biodiversity of the region; (2) addressed farming practices to minimize impact to the remaining forest habitat; (3) developed teacher training programs to increase scientific literacy in the schools; (4) addressed pet trade issues for rural, urban, and enforcement authorities; and (5) partnered with educational entities to integrate this information into existing school curriculum and established programming.
One challenge facing cotton-top tamarins was the amount of wood that was harvested from the forest and consumed for firewood. It is estimated that globally, nearly 2.5 billion people consume firewood, charcoal, crop residues, and dung as their primary source of energy. In discussions with local villagers in Colombia, we discovered the traditional Colombian ‘‘binde’’ a small cook stove that was made from a termite mound. Interviews with local villagers indicated that bindes required less firewood than cooking over an open fire. Although accepted by local communities in Colombia, there were limitations with bindes made from termite mounds because they often cracked and disintegrated with repeated use. Given that bindes were already a part of the culture; our goal was to make bindes better. We designed a durable binde made of clay. A family of five used approximately 15 logs a day to cook their food over an open fire but using a binde, the number of logs consumed each day was reduced by 2/3rds.
In December 2008, a survey was administered to 107 families that had received a binde. All 107 individuals that participated in the survey were still using the binde they received in 2006. Although 57% of these original bindes had cracks or were slightly damaged during the 2-year study, they were still in use. One hundred percent of the respondents believed that they used less fuel when cooking in a binde than over an open fire and they estimated a 50% reduction in firewood needed annually for cooking. Our studies have suggested that communities readily used bindes and found them to be of value, and also were cutting fewer trees in the forest.
Regardless of effectiveness of the conservation education programs, our experience has shown that if basic human needs are not met, local communities will not engage in activities that positively benefit wildlife. Our goal was to create an artisan group that would create a product from plastic bags that were littering the environment and jeopardizing the future survival of cotton-top tamarins. By providing a stable source of income to the artisan group combined with effective conservation education messaging, they would then commit to protecting the forests and not capture cotton-top tamarins for the illegal pet trade. Today, the artisans have a thriving business selling a variety of products crocheted from plastic bags.
This type of collaborative approach that combines educational programs that increase awareness to the plight of the cotton-top tamarin with opportunities for direct economic benefit results in creating new local champions that are committed to protecting these resources for the future.