Impending extinction crisis of the world's primates: Why primates matter.

Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.

Paternity in wild ring-tailed lemurs (Lemur catta): Implications for male mating strategies.

In group-living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single-male monopolization of paternity in groups. Ring-tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi-male, multi-female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra-group males-posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80-95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra-troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra-group mating is a viable strategy that can result in extra-group paternity for L. catta males.

Behavioral thermoregulation in Lemur catta: The significance of sunning and huddling behaviors.

Regulation of body temperature poses significant problems for organisms that inhabit environments with extreme and seasonally fluctuating ambient temperatures. To help alleviate the energetic costs of autonomic responses, these organisms often thermoregulate through behavioral mechanisms. Among primates, lemurs in Madagascar experience uncharacteristically seasonal and unpredictable climates relative to other primate-rich regions. Malagasy primates are physiologically flexible, but different species use different mechanisms to influence their body temperatures. Lemur catta, the ring-tailed lemur, experiences particularly acute diurnal temperature fluctuations in its mostly open-canopy habitat in south and southwest Madagascar. Ring-tailed lemurs are also atypical among lemurs in that they appear to use both sun basking postures and huddling to maintain body temperature when ambient temperatures are cold. To our knowledge, however, no one has systematically tested whether these behaviors function in thermoregulation. We present evidence that ring-tailed lemurs use these postures as behavioral thermoregulation strategies, and that different environmental variables are associated with the use of each posture. Major predictors of sunning included ambient temperature, time of day, and season. Specifically, L. catta consistently assumed sunning postures early after daybreak when ambient temperatures were <13°C, and ceased sunning around 10:00a.m., after ambient temperatures approached 26°C. Sunning occurred more often during austral winter months. Huddling was associated with time of day, but not with ambient temperature or season. We conclude that L. catta tend to sun, rather than huddle, under cold weather conditions when sunning is possible. However, both sunning and huddling are important behavioral adaptations of L. catta that augment chemical thermoregulation and the absence of a dynamic, insulating pelage. Sunning and huddling help to account for the great ecological flexibility of the species, but these adaptations may be insufficient in the face of future changes in protective vegetation and temperature. Am. J. Primatol. 78:745-754, 2016. © 2016 Wiley Periodicals, Inc.

Comparison of the genetic variation of captive ring-tailed lemurs with a wild population in Madagascar.

Genetic variability among captive and wild ring-tailed lemurs (Lemur catta) was assessed using mitochondrial and nuclear DNA data. A 529 bp segment of mtDNA was sequenced and 9 microsatellite loci were genotyped for 286 ring-tailed lemurs. Samples were obtained from the well-studied L. catta population at the Bezà Mahafaly Special Reserve and from captive animals at six institutions worldwide. We found evidence of possible patrilineal contribution but the absence of matrilineal contribution from the Bezà area, and haplotypes not found in Bezà but present in Ambohimahavelona, Andringitra Massif, and other unknown locations, in the sampled captive population, indicating that the founders of the captive population originated from a wide geographic range. Total genetic variation and relatedness in captive L. catta in the six institutions were similar in extent to that of the wild population in Bezà. Based on the diverse origins of the captive population founders our results suggest the erosion of genetic diversity in the captive population. Sampled individuals from the same institution were more closely related to each other than members of a social group in the wild. Individuals housed at different institutions were less closely related than those of different social groups at Bezà, indicating lower genetic exchange between captive institutions than between social groups in a locality in the wild. Our findings underscore the usefulness of genotyping in determining the geographic origin of captive population founders, obtaining pedigree information if paternity is uncertain, and in maximizing preservation of extant genetic diversity in captivity.

Genetic Evidence for Male and Female Dispersal in Wild Lemur catta.

Lemur catta has traditionally been considered a species with male-biased dispersal; however, occasional female dispersal occurs. Using molecular data, we evaluated dispersal patterns in 2 L. catta populations in southwestern Madagascar: Tsimanampesotse National Park (TNP) and Bezà Mahafaly Special Reserve (BMSR). We also investigated the genetic differentiation between the populations and dispersal partner relatedness. Results showed minor genetic differentiation between the populations (Ï´(ST) = 0.039), which may indicate gene flow historically occurring in this region, made possible by the presence of L. catta groups between the sites. Different patterns of sex-biased dispersal were found between the sites using corrected assignment indices: male-biased dispersal in TNP, and a lack of sex-biased dispersal in BMSR. Observational evidence of female dispersal in BMSR supports these results and may imply intense female resource competition in and around BMSR, because small groups of 2-3 females have been observed dispersing within BMSR and entering the reserve from outside. These dispersing groups largely consisted of mothers transferring with daughters, although we have an aunt-niece pair transferring together. Genetic data suggest that males also transfer with relatives. Our data demonstrate that dispersal partners consist of same-sexed kin for L. catta males and females, highlighting the importance of kin selection.

The role of piloerection in primate thermoregulation.

The insulating properties of the primate integument are influenced by many factors, including piloerection, which raises the hair and insulates the body by creating motionless air near the skin's surface. The involuntary muscles that control piloerection, the musculi arrectores pilorum (MAP), are mostly absent except on the tail in most strepsirhines, and are entirely absent in tarsiers and some lorisids. The absence of piloerection and the reduced effectiveness of pilary insulation in preventing heat loss affected the evolution of behavior and metabolic thermoregulation in these animals. In lemurs, this situation contributed to the use of positional and social behaviors such as sunning and huddling that help maintain thermal homeostasis during day-night and seasonal temperature cycles. It also contributed in many lemurs and lorises to the evolution of a wide variety of activity patterns and energy-conserving metabolic patterns such as cathemerality, daily torpor, and hibernation. The absence of functional MAP in strepsirhines and tarsiers implies the absence of effective piloerection in early primates, and the reacquisition of whole-body MAP in ancestral anthropoids prior to the separation of platyrrhine and catarrhine lineages. © 2013 S. Karger AG, Basel.

Rethinking primate origins again.

In 1974, Cartmill introduced the theory that the earliest primate adaptations were related to their being visually oriented predators active on slender branches. Given more recent data on primate-like marsupials, nocturnal prosimians, and early fossil primates, and the context in which these primates first appeared, this theory has been modified. We hypothesize that our earliest primate relatives were likely exploiting the products of co-evolving angiosperms, along with insects attracted to fruits and flowers, in the slender supports of the terminal branch milieu. This has been referred to as the primate/angiosperm co-evolution theory. Cartmill subsequently posited that: "If the first euprimates had grasping feet and blunt teeth adapted for eating fruit, but retained small divergent orbits…" then the angiosperm coevolution theory would have support. The recent discovery of Carpolestes simpsoni provides this support. In addition, new field data on small primate diets, and a new theory concerning the visual adaptations of primates, have provided further evidence supporting the angiosperm coevolution theory.

Variation in dental wear and tooth loss among known-aged, older ring-tailed lemurs (Lemur catta): a comparison between wild and captive individuals.

Tooth wear is generally an age-related phenomenon, often assumed to occur at similar rates within populations of primates and other mammals, and has been suggested as a correlate of reduced offspring survival among wild lemurs. Few long-term wild studies have combined detailed study of primate behavior and ecology with dental analyses. Here, we present data on dental wear and tooth loss in older (>10 years old) wild and captive ring-tailed lemurs (Lemur catta). Among older ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar (n=6), the percentage of severe dental wear and tooth loss ranges from 6 to 50%. Among these six individuals, the oldest (19 years old) exhibits the second lowest frequency of tooth loss (14%). The majority of captive lemurs at the Indianapolis Zoo (n=7) are older than the oldest BMSR lemur, yet display significantly less overall tooth wear for 19 of 36 tooth positions, with only two individuals exhibiting antemortem tooth loss. Among the captive lemurs, only one lemur (a nearly 29 year old male) has lost more than one tooth. This individual is only missing anterior teeth, in contrast to lemurs at BMSR, where the majority of lost teeth are postcanine teeth associated with processing specific fallback foods. Postcanine teeth also show significantly more overall wear at BMSR than in the captive sample. At BMSR, degree of severe wear and tooth loss varies in same aged, older individuals, likely reflecting differences in microhabitat, and thus the availability and use of different foods. This pattern becomes apparent before "old age," as seen in individuals as young as 7 years. Among the four "older" female lemurs at BMSR, severe wear and/or tooth loss do not predict offspring survival.

Effects of food, proximity, and kinship on social behavior in ringtailed lemurs.

Efforts to understand the variation in primate social systems and their underlying interaction patterns have focused on both intrinsic and extrinsic factors. In the socioecological model, food distribution and abundance have been argued to be the primary influences on the social behavior of primate species. We examined the relationship of food resources and two intrinsic factors-kinship and proximity-with patterns of affiliative and agonistic relationships in two semi-free ranging ringtailed lemur, Lemur catta, social groups (N=14) at The Duke Lemur Center in Durham, NC. In analyzing these three factors concurrently within the same system, we attempt to establish their relative power in explaining the characteristics of social relationships. Patterns of affiliation and high-intensity agonism were best explained by kinship. Proximity also explained affiliation but did not explain agonism, which varied considerably between groups. The influence of food on social interactions was highly variable between the two groups and, therefore, did not convincingly account for the social behavior patterns we observed. Finally, different intensities of agonism have different patterns and should be analyzed individually. The variation between social groups makes it difficult for us to conclude that any one factor is primarily and universally responsible for patterns of social behavior in this species.

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar.

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.

An academic genealogy on the history of American field primatologists.

In this paper, we present the academic genealogy of American field primatologists. The genealogy has been compiled to formally document the historical record of this young field. Data have been collected from three main sources: 1) e-mail surveys, 2) library and Internet research, and 3) verbal communication through forums such as American Association of Physical Anthropology meetings. Lineages of primatologists have been graphically displayed using Microsoft Visio. As of September 2005, 672 names and 239 affiliated universities, organizations and institutions have been recorded in 19 lineages. Five hundred and thirty-eight of the 672 names, 80.1%, are field primatologists. The Hooton/Washburn lineage is the largest; 60.6% of the recorded field primatologists are linked to this lineage. In addition, four of the five professors who have mentored a comparable number of field primatologists at American universities since Washburn are linked to the Hooton/Washburn lineage; and the school where Washburn mentored a majority of his students, UC-Berkeley, continues to have the highest overall graduation record for this subdiscipline. However, the field of primatology has been diversifying since the 1960s, and different universities are now responsible for graduating a substantial number of primatologists. We conclude that while the Hooton/Washburn lineage has remained remarkably homogenous in its anthropological focus, the field is also becoming increasingly enriched by primatologists who have had training in fields such as zoology, psychology, and ecology both in the United States and abroad.

Personality traits in captive lion-tailed macaques (Macaca silenus).

Personality influences an individual's perception of a situation and orchestrates behavioral responses. It is an important factor in elucidating variation in behavior both within and between species. The major focus of this research was to test a method that differs from those used in most previous personality studies, while investigating the personality traits of 52 captive lion-tailed macaques from four zoos. In this study, data from behavioral observations, a P-type principal components analysis (PCA), and bootstrapped confidence intervals as criteria for judging the significance of factor loadings were used rather than subjective ratings, R-type factor analyses, and arbitrary rules of thumb to determine significance. We investigated the relationships among individual component scores and sex, hormonal status, and dominance rank (controlling for age and social group) using a multiple regression analysis with bootstrapped confidence intervals. Three personality dimensions emerged from this analysis: Component 1 contained Extraversion-like behaviors related to sociability and affiliativeness. The higher mean Component score for females suggests that they are more "extraverted" than males. Only agonistic behaviors were significantly related to component 2. High-ranking individuals exhibited higher mean Component 2 scores than mid- or low-ranked individuals. Bold and cautious behaviors both loaded positively on Component 3, suggesting a dimension related to curiosity. The mean Component 3 score for females was higher than the mean score for males. The method used in this study should facilitate intraspecific and general interspecific comparisons. Developing a standardized trait term list that is applicable to many species, and collecting trait term data in the same manner and concurrent with behavioral observations (and physiologic measures when feasible) could prove useful in primate research and should be explored.

The value of radio tracking in the study of neotropical rain forest monkeys.

Although radio tracking has been used increasingly in primate field studies over the past 15 years, some primatologists have been reluctant to use it. We present data that demonstrate benefits of radio tracking in the study of rain forest primates. Data were collected during an ecological study of Ateles geoffroyi and Cebus capucinus in hilly, dense rain forest habitat with poor visibility, in northeastern Costa Rica. We SHOW that radio tracking decreased search time for both species, which led to increased contact time and facilitated continuous data collection. Mean search time for both primate species was significantly reduced using radio tracking (Kruskal-Wallis Test, P < 0.05). Search times for both species increased at the end of the study, when the transmitters ceased functioning. These increased search times occurred despite high levels of familiarity with the ranging patterns of the animals. The rate of marking feeding trees increased significantly with radio tracking and decreased significantly when the radios failed (Kruskal-Wallis Test, P < 0.01). Other benefits of radio tracking include: finding animals far off trail, in dense vegetation, and in inclement weather; maintaining continuous contact with the animals, which allows for more complete knowledge of ranging and foraging patterns; and monitoring group and subgroup composition. © 1994 Wiley-Liss, Inc.

Primate origins and the evolution of angiosperms.

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.