Golden lion tamarin metapopulation dynamics five years after heavy losses to yellow fever.

The golden lion tamarin (GLT) is an Endangered primate endemic to Brazil's lowland Atlantic Forest. After centuries of deforestation and capture for the pet trade, only a few hundred individuals survived, all in isolated forest fragments 85 km from Rio de Janeiro city. Intensive conservation actions, including reintroduction of zoo-born tamarins, increased numbers to about 3700 in 2014. The most severe yellow fever epidemic/epizootic in Brazil in 80 years reduced two of the largest GLT populations by over 90%. Herein we report the results of a 2023 survey of GLTs designed to examine the dynamics of population recovery following yellow fever. Results indicate that populations hard hit by yellow fever are recovering due in part to immigration from adjacent forest fragments. No local extirpations were observed. About 4800 GLTs live in the survey area. This represents a 31% increase since the baseline survey completed in 2014. Two factors explain most of the increase: four large areas that had no GLTs or very low-density populations in 2014 are now at moderate density (three areas) or low density (one area), explaining 71% of overall increase since 2014. Increase in forest area within our survey area may explain up to 16% of the increase in GLT numbers since 2014. Results of computer simulations suggest that strengthening forest connectivity will facilitate metapopulation resilience in the face of mortality factors such as yellow fever.

Yellow fever in Brazil threatens successful recovery of endangered golden lion tamarins.

The golden lion tamarin is an endangered primate endemic to Brazil's Atlantic Forest. Centuries of deforestation reduced numbers to a few hundred individuals in isolated forest fragments 80 km from Rio de Janeiro city. Intensive conservation action including reintroduction of zoo-born tamarins into forest fragments 1984-2000, increased numbers to about 3,700 in 2014. Beginning in November 2016, southeastern Brazil experienced the most severe yellow fever epidemic/epizootic in the country in 80 years. In May 2018, we documented the first death of a golden lion tamarin due to yellow fever. We re-evaluated population sizes and compared them to results of a census completed in 2014. Tamarin numbers declined 32%, with ca. 2,516 individuals remaining in situ. Tamarin losses were significantly greater in forest fragments that were larger, had less forest edge and had better forest connectivity, factors that may favor the mosquito vectors of yellow fever. The future of golden lion tamarins depends on the extent of additional mortality, whether some tamarins survive the disease and acquire immunity, and the potential development of a vaccine to protect the species against yellow fever.

Estimating population sizes to evaluate progress in conservation of endangered golden lion tamarins (Leontopithecus rosalia).

Efforts to reverse the decline of endangered golden lion tamarin monkeys have been relatively successful because the Brazilian organization dedicated to the species' conservation (Associação Mico-Leão-Dourado, AMLD) relies on science-based computer modeling to determine the number of tamarins necessary to achieve demographic and genetic goals, and a process of strategic planning to achieve those goals. Accurate estimates of the numbers of tamarins in forest fragments are essential to evaluate progress in achieving goals and adapt strategies as necessary. In this report we present the results of a new method to survey the number of tamarins in the wild, a modification of the point transect with lures procedure. Using this method, we estimate that in 2014 there were approximately 3,700 golden lion tamarins in 41,400 hectares of Atlantic Forest. Of these, 59% are from remnant wild populations, 34% are descendants of captive-born reintroduced animals and 7% are descendants of wild translocated groups. The number of tamarins and amount of forest estimated in this survey exceeded values necessary to meet AMLD's definition of a viable population, determined to be 2,000 tamarins in 25,000 hectares of connected and protected forest. However, the seven forest blocks and their tamarin populations are not yet adequately connected and protected. AMLD's strategic plan to achieve a viable population of golden lion tamarins includes 12 strategies that mitigate these and other threats or contribute directly to the conservation goal. The point transect with lures survey method provides a way to evaluate progress in achieving that goal and adapt strategies as appropriate.

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.

Tree and forest characteristics influence sleeping site choice by golden lion tamarins.

Lion tamarin monkeys are among a small number of primates that repeatedly use a few tree holes for the majority of their sleeping sites. To better understand why lion tamarins rely on tree holes as sleeping sites, we compared the physical characteristics of frequently used sleeping sites, infrequently used sleeping sites, and randomly selected forest locations at multiple spatial scales. From 1990 to 2004, we recorded 5,235 occurrences of sleeping site use by 10 groups of golden lion tamarins (Leontopithecus rosalia) in Poço das Antas Reserve, Rio de Janeiro State, Brazil. Of those, 63.6% were tree holes. Bamboo accounted for an additional 17.5% of observations. Frequently used tree holes were more likely to be found in living trees and their entrances were at lower canopy heights than infrequently used tree holes. We also found that frequently used sleeping sites, in comparison to random sites, were more likely to be found on hillsides, be close to other large trees, have a lower percent of canopy cover, and have larger diameter at breast height. Topography and small-scale variables were more accurate than were habitat-level classifications in predicting frequently used sleeping sites. There are ample tree holes available to these lion tamarins but few preferred sites to which they return repeatedly. The lion tamarins find these preferred sites wherever they occur including in mature forest and in relics of older forest embedded in a matrix of secondary forest.

Golden lion tamarin sleeping-site use and pre-retirement behavior during intense predation.

Sleeping sites, their patterns of use, and cryptic pre-retirement behavior mitigate predation risk at sleeping sites and could influence prey fitness. We evaluated sleeping-site usage for 10 groups of golden lion tamarins (GLTs) from a population that recently suffered a substantial decline due to predation at sleeping sites. We recorded the average number of nights that groups spent at their different sleeping sites to determine whether patterns of sleeping-site use were influenced by predation risk, as measured by the rate of encounters with predators, or the availability of suitable sleeping sites, as measured by the size of a group's home range and amount of mature forest within their home range. In addition, we measured travel speed to sleeping sites and compared this speed with that recorded at other times of day. GLT groups spent more nights on average at each of their sleeping sites compared to other callitrichid species for which data are available. Predation risk and habitat characteristics were not significant predictors of how many times groups used each of their different sleeping sites. Groups significantly increased their travel speed just before entering the sleeping site. Rapid locomotion to secure tree cavities may help GLTs avoid crepuscular and nocturnal predators; however, we speculate that this strategy failed numerous GLTs in our study population during the previous decade because they used sleeping sites that were accessible to predators.

Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi).

Limited data are available on the long-term effect an encounter with a predator has on its potential prey. Anecdotal reports from field research indicate that even unsuccessful attacks by predators on callitrichids have long-lasting effects. The subjects for this study were two groups of Geoffroy's marmosets (Callithrix geoffroyi) housed outside, off exhibit, at the Center for Reproduction of Endangered Species at the San Diego Wild Animal Park. Before they retired in the evening, the marmosets were observed under one of three conditions: snake model, cloth control, and no-stimulus control. Data were collected the following morning for 1 hr after the animals emerged from the sleeping box. Compared to control conditions, exposure to the snake model before retirement the previous evening was associated with significantly more vigilance checks (i.e., inspecting the area where the stimulus was last seen), and a delay in beginning to forage on the ground. These results suggest that callitrichids use recent threatening experiences to guide their vigilance behavior 12 hr after the threat is detected, and that they adjust their early morning behavior in response to potential predatory threats.