Stacey R. Tecot

Frugivory in four sympatric lemurs: implications for the future of Madagascar's forests.

Although some conservationists accept that not all species can be saved, we illustrate the difficulty in deciding which species are dispensable. In this article, we examine the possibility that the integrity of a forest relies on its entire faunal assemblage. In Madagascar, one faunal group, the lemurs, accounts for the greatest biomass and species richness among frugivores. For example, 7 of the 13 sympatric lemur species in Madagascars eastern rainforests consume primarily fruit. Because of this, we suggest that some tree species may rely heavily on particular lemur taxa for both seed dispersal and germination. In Ranomafana National Park, the diets for four of the day‐active lemur frugivores have been documented during annual cycles over a 5‐year period. We predicted that, although the fruit of some plant taxa would be exploited by multiple lemur species, the fruit of others would be eaten by one lemur species alone. Analyses reveal that while lemurs overlap in a number of fruit taxa exploited, 46% (16/35) of families and 56% (29/52) of genera are eaten exclusively by one lemur species. We, therefore, predict local changes in forest composition and structure if certain of these lemur species are eliminated from a forest owing to hunting, disease, or habitat disturbance. We also suggest that this result may be of global significance because carbon sequestration by the tropical forests in Madagascar may be reduced as a result of this predicted change in forest composition. Am. J. Primatol. 73:585–602, 2011.

Long-Term Lemur Research at Centre Valbio, Ranomafana National Park, Madagascar

We present findings from 25 years of studying 13 species of sympatric primates at Ranomafana National Park, Madagascar. Long-term studies have revealed that lemur demography at Ranomafana is impacted by climate change, predation from raptors, carnivores, and snakes, as well as habitat disturbance. Breeding is seasonal, and each species (except Eulemur rubriventer) gives birth synchronously to be able to wean before winter. Infant mortality is high (30–70%) and partly due to infanticide in Propithecus edwardsi,and perhaps Varecia variegata. Diurnal lemurs can live beyond 30 years in the wild and most females reproduce until death. Small-bodied Microcebus rufuslive up to 9 years without signs of senescence. Prolemur simusmigrates in search of new bamboo and mates, and related V. variegatamothers park their multiple offspring in “kindergartens,” protected by others while mothers forage. Interference competition among sympatric lemurs occurs. Anthropogenic factors, such as past selective logging and climate change may influence the declining density of E. rufifrons, P. simus, and P. edwardsiwhile not affecting the density of pair-living species.

Social Pair-Bonding and Resource Defense in Wild Red-Bellied Lemurs (Eulemur rubriventer)

Pair-bonding among nonhuman primates is rare and the possible selection pressures at work to maintain this type of social grouping have been discussed at great length (Kleiman, 1977; Wittenberger, 1980; Kinzey, 1987; Palombit, 1999; Fuentes, 1999, 2002; Chambers, 2002; Reichard, 2003; van Schaik and Kappeler, 2003). While the behavioral ecology of pair-bonded species has been relatively well studied across radiations, there are fewer studies that examine the nuances of social behavior between pair-bonded individuals and how social behavior is affected by ecological variables such as changes in food availability and feeding competition (but see Curtis and Zaramody, 1997; Bartlett, 2003; Fietz, 2003; Curtis, 2004; Schulke, 2003, 2005). This inhibits researchers’ ability to fully evaluate the two main competing hypotheses, mate defense and resource defense (Wrangham, 1980; Dunbar, 1988), that have been put forward to explain the evolution of pair-bonding. Of these two sets of hypotheses, mate defense models have received more attention and empirical support (van Schaik and Dunbar,

Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories

Allomaternal care is a rare, though phylogenetically widespread, mammalian infant care strategy. Among primates, the effects of allomaternal care are marked; its presence correlates with faster infant growth, younger age at weaning, and shorter interbirth intervals. Recent comparative research has found that such fertility benefits are absent in other mammals and are thus unique to primates. In large part because data describing lemur allomaternal care were lacking, the reproductive advantages of allomaternal care have never been demonstrated in Malagasy strepsirrhines. Using newly available data and rigorous phylogenetic methods, we extend this hypothesis to strepsirrhines and test whether allomaternal care in lemurs confers similar maternal reproductive benefits. Contrary to expectations, the presence of allomaternal care did not significantly impact lemur reproductive output; we did not find relationships between allomaternal care and either fetal or postnatal growth rates or interbirth intervals. Rather, infant parking and nesting, strategies employed primarily by litter-bearing species, were positively associated with faster fetal and postnatal infant growth, while nesting was negatively associated with interbirth interval. Thus, although each form of haplorrhine allomaternal care is also observed in Malagasy primates, the effects that these behaviors have on female reproductive output more closely resemble nonprimate mammals. We suggest that Malagasy strepsirrhines may not equally benefit from allomaternal care compared to haplorrhines because reproductive rates are less flexible and allomaternal care may instead increase infant survival in Madagascar’s harsh and unpredictable environment. Our study has significant implications for understanding the evolution of infant care and developmental trajectories in mammals.

Morphometrics and pattern of growth in wild sifakas (Propithecus edwardsi) at ranomafana national park, madagascar

We summarize morphometric data collected over a period of 22 years from a natural population of rainforest sifakas (Propithecus edwardsi) at Ranomafana National Park, Madagascar, and we use those data to document patterns of growth and development. Individually identified, known‐age sifakas were successfully captured, measured, and released. We found that body segment lengths increased faster during growth than did body mass, with individuals attaining adult lengths earlier than adult mass. Females can begin reproducing before they are fully grown, but this may not be common. With the exception of hand length, we found no significant sex difference in any adult metric including body mass, chest, and limb circumferences, body segment lengths, and canine tooth height; however, body masses of individual females fluctuated more, independently of pregnancy, than did those of males. We found considerable interannual fluctuation in body mass with single individuals differing more within the same season in different years than from season to season in the same year. Such body mass fluctuation may be a consequence of eastern Madagascars variable and unpredictable environment in which rainfall during any selected month varies from year to year. Am. J. Primatol. 73:155–172, 2011.

Why "monogamy" isn't good enough.

Rare in mammals but more common in primates, there remains a considerable controversy concerning whether primate species traditionally described as monogamous actually express this highly specialized breeding pattern. Unfortunately the definition of “monogamy” varies greatly, inhibiting our understanding of this trait and two related traits with which monogamy is often conflated: pair‐living and pair‐bonding. Strepsirrhine primates are useful models to study factors that select for pair‐living, pair‐bonding, and monogamy because this taxon exhibits high incidences of each trait, in addition to species that exhibit behaviors that reflect combinations of these traits. Several hypotheses have been articulated to help explain the evolution of “monogamy,” but again, these hypotheses often conflate pair‐living, pair‐bonding, and/or monogamy. In this review, we (1) propose clear, discrete, and logical definitions for each trait; (2) review variation in strepsirrhines with respect to these three traits; (3) clarify which of these traits can be explained by existing hypotheses; and (4) provide an example of the applicability of the Resource Defense Hypothesis (RDH) to understand two of these traits, pair‐living and pair‐bonding, in the red‐bellied lemur (Eulemur rubriventer). Available data support the RDH for pair‐living in red‐bellied lemurs. They live in stable family groups with one adult pair. Both sexes actively codefend territories that overlap little with other pairs’ territories. Agonism is extremely rare within groups and intergroup and interspecific agonism varies with food availability. Available data also support the RDH for pair‐bonding. Pair‐bonds are cohesive year‐round. Pairs coordinate behaviors to defend territories with auditory and olfactory signals. Cohesion increases with food abundance and both sexes reinforce bonds. We indicate where additional data will help to more rigorously test the RDH for each trait and encourage others to test alternative hypotheses. Am. J. Primatol. 78:340–354, 2016.

Teeth, Sex, and Testosterone: Aging in the World's Smallest Primate

Mouse lemurs (Microcebus spp.) are an exciting new primate model for understanding human aging and disease. In captivity, Microcebus murinus develops human-like ailments of old age after five years (e.g., neurodegeneration analogous to Alzheimers disease) but can live beyond 12 years. It is believed that wild Microcebus follow a similar pattern of senescence observed in captive animals, but that predation limits their lifespan to four years, thus preventing observance of these diseases in the wild. Testing whether this assumption is true is informative about both Microcebus natural history and environmental influences on senescence, leading to interpretation of findings for models of human aging. Additionally, the study of Microcebus longevity provides an opportunity to better understand mechanisms of sex-biased longevity. Longevity is often shorter in males of species with high male-male competition, such as Microcebus, but mouse lemurs are sexually monomorphic, suggesting similar lifespans. We collected individual-based observations of wild brown mouse lemurs (Microcebus rufus) from 2003–2010 to investigate sex-differences in survival and longevity. Fecal testosterone was measured as a potential mechanism of sex-based differences in survival. We used a combination of high-resolution tooth wear techniques, mark-recapture, and hormone enzyme immunoassays. We found no dental or physical signs of senescence in M. rufus as old as eight years (N = 189, ages 1–8, mean = 2.59±1.63 SE), three years older than captive, senescent congeners (M. murinus). Unlike other polygynandrous vertebrates, we found no sex difference in age-dependent survival, nor sex or age differences in testosterone levels. While elevated male testosterone levels have been implicated in shorter lifespans in several species, this is one of the first studies to show equivalent testosterone levels accompanying equivalent lifespans. Future research on captive aged individuals can determine if senescence is partially a condition of their captive environment, and studies controlling for various environmental factors will further our understanding of senescence.

Reproductive Strategies and Infant Care in the Malagasy Primates

The old African proverb, “It takes a village to raise a child,” may extend well beyond the collective effort attributed to human child rearing strategies. In fact, allomaternal care is taxonomically widespread, particularly among mammalian taxa (e.g., rodents: Gubernick and Alberts 1987; Solomon and Getz 1997; chiroptera: O’Farrell and Studier 1973; canids: Moehlman and Hofer 1997; cetaceans: Gero et al. 2009; and primates: Hrdy 1976; Chism 2000). Allomaternal care includes infant care provided by the father (paternal care, Fernandez-Duque et al. 2009) or by conspecifics other than the parents (alloparental care, Wilson 1975). While well represented by a diversity of taxa, allomaternal care is not common among mammals (e.g., 9–10% of taxa display paternal care; Kleiman and Malcolm 1981; Huck and Fernandez-Duque 2012), allomaternal care has been recently noted to occur at relatively high frequencies in the Order Primates, particularly among many haplorhine (e.g., monkey and ape) species (Tardif 1997; Chism 2000; Ross and MacLarnon 2000; Hrdy 2009). While studies have examined the causes and consequences of allomaternal care among haplorhines, to our knowledge, there has yet to be a comprehensive analysis of allomaternal care across the entire primate order (e.g., including the primates of Madagascar, hereafter referred to as lemurs). This is in large part because studies of lemur allomaternal care have lagged behind those of their primate cousins. The most recent attempt at a synthesis of primate allomaternal care found that it was a haplorhine-biased phenomenon, finding no evidence of lemurs participating in allomaternal care-related behaviors (Ross 2003), and thus precluding any analysis of allomaternal care within that taxon. However, recent increases in attention to and sampling effort of lemur care behaviors have revealed that allomaternal care is more common in lemurs than originally thought (Mitchell 1969; Klopfer 1974; Pereira et al. 1987; Wright 1990; Patel 2007; Hrdy 2010; Rowe and Myers 2011; Tecot and Hrdy, unpublished data). Moreover, a number of studies in recent years have added to our understanding of this postnatal care strategy in lemurs, making it possible to include these species in broader taxonomic comparisons of primate reproductive strategies. In light of these recent discoveries, we aim to (1) describe the different types of allomaternal care observed in primates, including a discussion of how each type of care is expressed in monkeys and apes, and a summary of what is currently known for lemurs; (2) discuss the benefits of allomaternal caretaking and whether such behaviors benefit lemur mothers; and (3) outline important gaps in our knowledge of lemur allomaternal care, suggesting future avenues of research.

Lemur Habitat and Dental Senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.

Anthropogenic and Climatic Effects on the Distribution of Eulemur Species: An Ecological Niche Modeling Approach

Several factors can influence primate distributions, including evolutionary history, interspecific competition, climate, and anthropogenic impacts. In Madagascar, several small spatial scale studies have shown that anthropogenic habitat modification affects the density and distribution of many lemur species. Ecological niche models can be used to examine broad-scale influences of anthropogenic impacts on primate distributions. In this study, we examine how climate and anthropogenic factors influence the distribution of 11 Eulemur species using ecological niche models. Specifically, we created one set of models only using rainfall and temperature variables. We then created a second set of models that combined these climate variables with three anthropogenic factors: distance to dense settlements, villages, and croplands. We used MaxEnt to generate all the models. We found that the addition of anthropogenic variables improved the climate models. Also, most Eulemur species exhibited reduced predicted geographic distributions once anthropogenic factors were added to the model. Distance to dense settlements was the most important anthropogenic factor in most cases. We suggest that including anthropogenic variables in ecological niche models is important for understanding primate distributions, especially in regions with significant human impacts. In addition, we identify several Eulemur species that were most affected by anthropogenic factors and should be the focus of increased conservation efforts.