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.

Information seeking in western lowland gorillas (Gorilla gorilla gorilla).

Many animals will seek information when they do not know the answer to a problem, suggesting that they monitor their knowledge state. In the classic "tubes task," subjects are presented with a set of opaque tubes and either see (visible trials) or do not see (hidden trials) which tube holds a food reward on a given trial. Chimpanzees, bonobos, orangutans, and human children show information-seeking behavior on this task, looking into the tubes to find the reward more on hidden than on visible trials. However, evidence for information-seeking behavior in gorillas is limited. In Experiment 1, gorillas that were presented with a classic information-seeking tubes task showed performance patterns consistent with metacognitive behavior; they looked down tubes more on hidden than on visible trials, their accuracy on hidden trials on which they looked was higher than on hidden trials on which they did not look, and they primarily employed an appropriate search strategy when looking down the tubes. In Experiment 2, we decreased or increased the amount of effort required to look down the tubes by increasing or decreasing the height of the tubes, respectively. Gorillas were less likely to look in tubes on trials that required high effort, but continued to look more on hidden than on visible trials, indicating that their tendency to look was affected by both knowledge state and effort. Together these results provide strong evidence for logical, controlled information-seeking behavior by gorillas.

After short interbirth intervals, captive callitrichine monkeys have higher infant mortality.

Life history theory predicts a trade-off between the quantity and quality of offspring. Short interbirth intervals-the time between successive births-may increase the quantity of offspring but harm offspring quality. In contrast, long interbirth intervals may bolster offspring quality while reducing overall reproductive output. Further research is needed to determine whether this relationship holds among primates, which have intensive parental investment. Using Cox proportional hazards models, we examined the effects of interbirth intervals (short, normal, or long) on infant survivorship using a large demographic dataset (n = 15,852) of captive callitrichine monkeys (marmosets, tamarins, and lion tamarins). In seven of the nine species studied, infants born after short interbirth intervals had significantly higher risks of mortality than infants born after longer interbirth intervals. These results suggest that reproduction in callitrichine primates may be limited by physiologic constraints, such that short birth spacing drives higher infant mortality.

Greater dependence on working memory and restricted familiarity in orangutans compared with rhesus monkeys.

The prefrontal cortex is larger than would be predicted by body size or visual cortex volume in great apes compared with monkeys. Because prefrontal cortex is critical for working memory, we hypothesized that recognition memory tests would engage working memory in orangutans more robustly than in rhesus monkeys. In contrast to working memory, the familiarity response that results from repetition of an image is less cognitively taxing and has been associated with nonfrontal brain regions. Across three experiments, we observed a striking species difference in the control of behavior by these two types of memory. First, we found that recognition memory performance in orangutans was controlled by working memory under conditions in which this memory system plays little role in rhesus monkeys. Second, we found that unlike the case in monkeys, familiarity was not involved in recognition memory performance in orangutans, shown by differences with monkeys across three different measures. Memory in orangutans was not improved by use of novel images, was always impaired by a concurrent cognitive load, and orangutans did not accurately identify images seen minutes ago. These results are surprising and puzzling, but do support the view that prefrontal expansion in great apes favored working memory. At least in orangutans, increased dependence on working memory may come at a cost in terms of the availability of familiarity.

Comparative performance of orangutans (Pongo spp.), gorillas (Gorilla gorilla gorilla), and drills (Mandrillus leucophaeus), in an ephemeral foraging task.

A goal of the comparative approach is to test a variety of species on the same task. Here, we examined whether the factors that helped capuchin monkeys improve their performance in a dichotomous choice task would generalize to three other primate species: orangutans, gorillas, and drill monkeys. In this task, subjects have access to two options, each resulting in an identical food, but one (the ephemeral option) is only available if it is chosen first, whereas the other one (the permanent option) is always available. Therefore, the food-maximizing solution is to choose the ephemeral option first, followed by the permanent option for an additional reward. On the original version (plate task), the options were discriminated by the color and pattern of the plates holding the food, while on two subsequent versions we used altered cues that we predicted would improve performance: (1) the color of the foods themselves (color task), which we hypothesized was relevant to primates, who choose foods rather than substrates on which foods are found when foraging, and (2) patterned cups covering the foods (cup task), which we hypothesized would help primates avoid the prepotent response associated with visible food. Like capuchins, all three species initially failed to solve the plate task. However, while orangutans improved their performance from the plate to the color task, they did not for the cup task, and only a few gorillas and no drills succeeded in either task. Unfortunately, our ability to interpret these data was obscured by differences in the subjects' level of experience with cognitive testing and practical constraints that precluded the use of completely identical procedures across species. Nonetheless, we consider what these results can tell us, and discuss the value of conducting studies across multiple sites despite unavoidable differences.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys.

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.

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.

Gene changes may minimize masculinizing and defeminizing influences of exposure to male cotwins in female callitrichine primates.

BACKGROUND: Sexual differentiation in female mammals can be altered by the proximity of male littermates in utero, a phenomenon known as the intrauterine position effect (IUP). Among simian primates, callitrichines (marmosets and tamarins) are likely candidates for IUP, since they exhibit obligate dizygotic twinning and fetuses share extensive vascularization in utero. In this paper, we determined whether female reproductive parameters are altered by gestating with a male twin and evaluated changes in genes associated with anti-Müllerian and steroid hormones in twinning callitrichine primates. METHODS: We assessed the impact of gestation with male cotwins on reproductive performance and survivorship in female marmosets (Callithrix) and lion tamarins (Leontopithecus), contrasting measures for females gestated with one or more littermates (M+) or no male littermates (0M). We compared targeted coding regions for genes involved in steroidal and anti-Müllerian hormone mediation of sexual differentiation for representatives of twinning callitrichines (Callithrix, Saguinus, and Leontopithecus) with closely related New World primates that produce single births (Saimiri and Callimico). RESULTS: IUP effects in females were absent in female callitrichine primates: age at first ovulation, average litter size, and the proportion of stillborn infants, and lifetime survivorship did not differ between M+ and 0M females. We documented multiple nonsynonymous substitutions in genes associated with steroid synthesis, transport, and cellular action (SRD5A2, CYP19A1, SHBG, and AR) and with anti-Müllerian hormone (AMH and AMHR2) in callitrichines. In the only callitrichine to produce single infants (Callimico), two genes contained nonsynonymous substitutions relative to twinning callitrichines (CYP19A1 and AMRHR2); these substitutions were identical with nontwinning Saimiri and humans, suggesting a reversion to an ancestral sequence. CONCLUSIONS: In spite of a shared placental vasculature with opposite-sex twins throughout embryonic and fetal development, female callitrichine primates gestated with a male cotwin exhibit no decrement in reproductive performance relative to females gestated with female cotwins. Hence, IUP effects on female reproduction in callitrichines are modest. We have identified mutations in candidate genes relevant for steroid hormone signaling and metabolism, and especially in AMH-related genes, that are likely to alter protein structure and function in the callitrichines. These mutations may confer protection for females from the masculinizing and defeminizing influences of gestating with a male cotwin.

Similar stimulus features control visual classification in orangutans and rhesus monkeys.

Many species classify images according to visual attributes. In pigeons, local features may disproportionately control classification, whereas in primates global features may exert greater control. In the absence of explicitly comparative studies, in which different species are tested with the same stimuli under similar conditions, it is not possible to determine how much of the variation in the control of classification is due to species differences and how much is due to differences in the stimuli, training, or testing conditions. We tested rhesus monkeys (Macaca mulatta) and orangutans (Pongo pygmaeus and Pongo abelii) in identical tests in which images were modified to determine which stimulus features controlled classification. Monkeys and orangutans were trained to classify full color images of birds, fish, flowers, and people; they were later given generalization tests in which images were novel, black and white, black and white line drawings, or scrambled. Classification in these primate species was controlled by multiple stimulus attributes, both global and local, and the species behaved similarly.