Figure 3 - available via license: Creative Commons Attribution 4.0 International
Content may be subject to copyright.
Propithecus coquereli life stages.: Data files contain information for individuals at all stages of life. Shown are (a) newborn (b) infant (c) juvenile (d) yearling (e) young adult (f) reproductive adult and (g) old adult Propithecus coquereli.
Source publication
Since its establishment in 1966, the Duke Lemur Center (DLC) has accumulated detailed records for nearly 4,200 individuals from over 40 strepsirrhine primate taxa-the lemurs, lorises, and galagos. Here we present verified data for 3,627 individuals of 27 taxa in the form of a life history table containing summarized species values for variables rel...
Similar publications
A shorter lifespan as a potential cost of high reproductive effort in humans has intrigued researchers for more than a century. However, the results have been inconclusive so far and despite strong theoretical expectations we do not currently have compelling evidence for the longevity costs of reproduction. Using Monte Carlo simulation, it is shown...
Citations
... catta: 32.7 years; P. coquereli: 30.6 years), but ring-tailed lemurs have a higher median longevity of individuals that survived at least 30 days than Coquerel's sifaka (L. catta: 17.6 years; P. coquereli: 10.0 years)(Zehr et al., 2014). ...
Insufficient physical activity is a major risk factor for cardiometabolic disease (i.e., unhealthy weight gain, heart disease, and diabetes) in humans and may also negatively affect health of primates in human care. Effects of physical activity on energy expenditure and cardiometabolic health are virtually unstudied in nonhuman primates. We investigated physical activity and metabolic markers in 15 adult ring-tailed lemurs (Lemur catta) and 11 Coquerel's sifakas (Propithecus coquereli) at the Duke Lemur Center during a period of low activity in winter when the animals were housed in buildings (with outdoor access) and a period of high activity when individuals were free-ranging in large, outdoor, forested enclosures. We compared body mass, blood glucose, triglycerides, HDL- and LDL-cholesterol, physical activity via accelerometry, and total energy expenditure (TEE) via the doubly labeled water method (in ring-tailed lemurs only) between both conditions. Both species were more active and had a lower body mass in summer. Ring-tailed lemurs had a higher TEE and lower triglyceride levels in summer, whereas sifaka had higher triglyceride levels in summer. Individuals that increased their activity more, also lost more body mass. Individuals that lost more body mass, also had a positive change in HDL-cholesterol (i.e., higher values in summer). Changes in activity were not associated with changes in markers of metabolic health, body fat percentage and TEE (both unadjusted and adjusted for body composition). Older age was associated with lower activity in both species, and decreased glucose in ring-tailed lemurs, but was otherwise unrelated to metabolic markers and, for ring-tailed lemurs, adjusted TEE. Overall, body mass was lower during summer but the increase in physical activity did not strongly influence metabolic health or TEE in these populations.
... The DLC also maintains a large collection of banked tissues, deriving from routine veterinary procedures and necropsies, amassed over the Center's 55-year history. Detailed records of life and medical history, reproduction, and social-group membership are digitally maintained [72]. ...
Age and sex have a profound effect on cytosine methylation levels in humans and many other species. Here we analyzed DNA methylation profiles of 2400 tissues derived from 37 primate species including 11 haplorhine species (baboons, marmosets, vervets, rhesus macaque, chimpanzees, gorillas, orangutan, humans) and 26 strepsirrhine species (suborders Lemuriformes and Lorisiformes). From these we present here, pan-primate epigenetic clocks which are highly accurate for all primates including humans (age correlation R = 0.98). We also carried out in-depth analysis of baboon DNA methylation profiles and generated five epigenetic clocks for baboons (Olive-yellow baboon hybrid), one of which, the pan-tissue epigenetic clock, was trained on seven tissue types (fetal cerebral cortex, adult cerebral cortex, cerebellum, adipose, heart, liver, and skeletal muscle) with ages ranging from late fetal life to 22.8 years of age. Using the primate data, we characterize the effect of age and sex on individual cytosines in highly conserved regions. We identify 11 sex-related CpGs on autosomes near genes (POU3F2, CDYL, MYCL, FBXL4, ZC3H10, ZXDC, RRAS, FAM217A, RBM39, GRIA2, UHRF2). Low overlap can be observed between age- and sex-related CpGs. Overall, this study advances our understanding of conserved age- and sex-related epigenetic changes in primates, and provides biomarkers of aging for all primates.
... Furthermore, our analysis showed that their life history even accelerated from the first to the second half of the three-decade-long study (captured by the first principal component in Fig. 4). Gray mouse lemurs also started reproducing relatively early (they reach sexual maturity within the first year of life) and exhibit a high reproductive output (captured by the second principal component in Fig. 4) of 1 to 2 litters per year with 2 offspring per litter (31,32). This life history, coupled with a large geographic variation in demographic rates (33), suggests that gray mouse lemurs can adapt demographically to variable environmental conditions, but a more variable environment may render the species prone to local extinction by increasing population fluctuations and thus the chance of small and nonviable population sizes. ...
Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.
... In 2022, 60 individuals of this species were being held in a small number of zoos around the world (ZIMS 2022), more than 50 in registered captive facilities in Madagascar, and even more held in illegal facilities that are not registered with the government Schaefer 2017, LaFleur et al. 2019). It is difficult to maintain healthy indriids in captivity (Zehr et al. 2014, Cassady et al. 2018. Sifakas in captivity outside of Madagascar (P. ...
... Sifakas in captivity outside of Madagascar (P. coquereli and P. coronatus) frequently suffer from gastrointestinal and diarrheal diseases, decreased longevity, low infant survivorship, and decreased reproductive success (Zehr et al. 2014, Cassady et al. 2018. ...
... Lemurs, the endemic primates of Madagascar, have been underrepresented in these comparative studies because of the limited number of long-term study sites (Jolly, 2012;Kappeler and Fichtel, 2012a;Sussman et al., 2012;Wright et al., 2012;Kappeler et al., 2017). They are nonetheless interesting for studies of reproductive senescence because they tend to live longer than most anthropoid primates of similar body mass, with a remarkable maximum longevity of over 30 years for mammals of < 10 kg, at least in captivity (Zehr et al., 2014). Lemurs also exhibit impressive interspecific variation in age at first reproduction, litter size and reproductive rates (Kappeler, 1995(Kappeler, , 1996Ross, 1998;Tecot et al., 2013), but patterns and drivers of intraspecific variation have not yet been studied in great detail. ...
... Representatives of two lemur families (Indriidae and Lemuridae) that evolved diurnal activity, group living and single births independently (Kappeler, 1998;Kappeler and Pozzi, 2019), thus resembling anthropoid primates in key life-history features, have been subjected to long-term field studies. The available published information about lemur reproductive senescence can be summarized as follows (for wild mouse lemurs see Rina Evasoa et al., 2018; for captive lemurs: Zehr et al., 2014). First, one study of Milne Edward's sifakas (Propithecus edwardsi) revealed that, although no overall effect of age on fertility could be found, offspring survival was significantly decreased in years with below-average rainfall during the lactation period, but the age classification in this study was based on estimates of tooth wear rather than known ages (Wright et al., 2008). ...
... Both species live in small multi-male, multi-female groups and feed on a broad range of fruits and leaves (Koch et al., 2017). Verreaux's sifakas are slightly larger than redfronted lemurs (2.9 vs. 2.2 kg), their groups are of similar size (6.1 vs. 5.4 individuals), female reproduction begins later (5 vs. 3 years), but both species typically produce singletons and can live well over 20 years (Richard et al., 2000(Richard et al., , 2002Fichtel, 2012a, 2016;Zehr et al., 2014). Despite female philopatry in both species, female Verreaux's sifakas occasionally emigrate into other groups (Kappeler and Fichtel, 2012a), and female redfronted lemurs very rarely succeed in immigrating into other groups after being evicted from their natal one (Kappeler and Fichtel, 2012b). ...
The relationship between age and reproductive performance is highly variable across species. Humans and some cetaceans exhibit an extreme form of reproductive senescence in that female reproduction ceases years or even decades before average life expectancy is reached. However, neither the existence of reproductive senescence in some taxa nor its absence in others is fully understood. Comparative data from other long-lived mammals may contribute to a more comprehensive understanding of the evolution of menopause, but data from wild primates, in particular, are scarce. We therefore investigated age-related female reproductive performance in two wild sympatric populations of Malagasy primates: Verreaux’s sifakas (Propithecus verreauxi) and redfronted lemurs (Eulemur rufifrons), which have a maximal longevity of more than 20 years. Based on 25 years of long-term demographic data, we extracted information on reproductive output of 38 female Verreaux’s sifakas and 42 female redfronted lemurs. We modeled variation in female reproductive performance and interbirth intervals as a function of age, the number of adult females within a group to account for female competition, and rainfall as a proxy for annual variation in food availability. We also compared our results for these two species with data on captive populations of the same two genera that are buffered from fluctuations in environmental variables. Our analyses disclosed statistical evidence for reproductive senescence in three out of four populations (captive Coquerel’s sifakas, wild redfronted lemurs, and captive red lemurs) but not for wild Verreaux’s sifakas. Compared to wild populations, reproductive senescence was therefore not less pronounced in captive animals, even though the latter are buffered from environmental adversities. In wild redfronted lemurs, mothers were more likely to give birth in years with more rainfall, but neither the number of co-resident females, nor annual rainfall did predict variation in the probability of giving birth in wild Verreaux’s sifakas. Thus, our study contributes valuable comparative information on reproductive senescence in a basal group of primates, and offers insights into the modulating effects of environmental, social and phylogenetic factors on patterns and dynamics of age-specific female reproduction.
... Natural history museums hold preserved biodiversity collections and associated specimen and ecological data that have long been recognized as an invaluable and irreplaceable resource for biodiversity research and society (Johnson et al. 2011, McLean et al. 2016, Funk 2018, Nelson and Ellis 2019, Watanabe 2019, Lendemer et al. 2020, NASEM 2020. Zoos and aquariums (hereafter, we use zoos to refer to both zoos and aquariums) hold living collections of animals and associated data on life history, demographics, pedigree (genealogy), genetics, physiology, morphology, and behavior but are not typically recognized for their value for biodiversity research (see Zehr et al. 2014 for exceptions, but see Conde et al. 2019, NASEM 2020. Despite the potential for synergy that is apparent in the complementary and nonoverlapping specimen and data types held in zoos and natural history museums, formal partnerships between these two institution types are uncommon. ...
Zoos and natural history museums are both collections-based institutions with important missions in biodiversity research and education. Animals in zoos are a repository and living record of the world's biodiversity, whereas natural history museums are a permanent historical record of snapshots of biodiversity in time. Surprisingly, despite significant overlap in institutional missions, formal partnerships between these institution types are infrequent. Life history information, pedigrees, and medical records maintained at zoos should be seen as complementary to historical records of morphology, genetics, and distribution kept at museums. Through examining both institution types, we synthesize the benefits and challenges of cross-institutional exchanges and propose actions to increase the dialog between zoos and museums. With a growing recognition of the importance of collections to the advancement of scientific research and discovery, a transformational impact could be made with long-term investments in connecting the institutions that are caretakers of living and preserved animals.
... A full list of individuals including sex, mass, and age at the time of the experiment is provided in Table S1. Young adults were defined as individuals that were between the minimum dam age at conception and two times the minimum dam age at conception for each species, and old adults were defined as individuals that had exceeded the maximum dam age at conception for the species based on the long-term dataset compiled on the DLC lemur colony by Zehr et al. (2014). Adults were all individuals that fell between these two categories. ...
The ability to safely ascend and descend is critical to the success of arboreal animals. Nonprimate mammals typically descend supports headfirst aided by their claws, but primates must rely on grasping, and use a variety of behaviors to move down within an arboreal environment, including headfirst and tailfirst descending. This study assesses hypothesized body mass limits on vertical headfirst descent and identifies approximate support orientations and diameters at which headfirst descent is ceased in a sample of nine strepsirrhines species ranging in mass from 0.06 to 4.5 kg. Species under 1 kg, arboreal quadrupeds Cheirogaleus medius and Microcebus murinus, and slow climber Nycticebus pygmaeus, always descended supports headfirst regardless of orientation and diameter as long as a grasp could be established. Arboreal quadrupedal species above 1 kg, Daubetonia madagascariensis, Eulemur coronatus, Eulemur mongoz, Lemur catta, and Varecia variegata differed in the orientation at which they ceased using headfirst descent and the types of alternative descending behaviors they employed. Lemur catta, a highly terrestrial species, started to employ tailfirst descents at 45° and completely stopped using headfirst descent on steeper and thicker supports. Other arboreal quadrupeds, D. madagascariensis, E. coronatus, E. mongoz, and V. variegata, began using tailfirst descent at 60°. The vertical clinging and leaping species Propithecus coquereli rarely engaged in above branch quadrupedalism, and individuals were observed using tailfirst descents on supports as shallow as 15°. This study shows the ways in which mass and anatomy may constrain use of headfirst descent through arboreal environments, and the alternate strategies strepsirrhine primates employ to descend.
... Indeed (Curtis and Zaramody 1999) reported births in October-November in Anjamena (ca. 60km South-West of Mariarano) while their gestation length is estimated around four months (Zehr et al. 2014). This was later supported by the fact that I did not observe any mating events during our observation period and more concretely by a report of the presence of few months old young in the same population in January 2018 (Bertrand Andriatsitohaina personal communication). ...
Animals exhibit an astonishing diversity of communicative systems, with substantial variation in both the nature and the number of signals they produce. Variation in communicative complexity has been conceptually and empirically attributed to social complexity and formalized as the “social-complexity hypothesis for communicative complexity” (SCHCC). Indeed, group-living animals face complex social environments where they engage in a wide range of interactions with different social partners triggering the need for transmission of a broader diversity of messages. In chapter I (Peckre et al. 2019), I review the literature on the current tests of the SCHCC, pointing out and discussing what I identified as the main gaps in the current state of the art. Specifically, three key issues emerged from my analysis. The first issue concerns the operational definition of the main variables, social and communicative complexity. Notably, when defining communicative complexity, most empirical tests of the SCHCC focus on a single modality (e.g., acoustic, visual, olfactory) whereas several good reasons exist for acknowledging the multimodal nature of both, signals and communicative systems in this framework. At the system level, focusing on only one modality may lead to over- or underestimation of the relationship between social and communicative complexity. The second issue relates to the fact that while numerous studies have highlighted a link between social and communicative complexity, their correlative nature does not permit conclusions about the direction of causality. Indeed, alternative hypotheses involving anatomical, phylogenetical, or ecological factors have also been proposed to explain the evolution of more complex forms of communication. Finally, I note that researchers rarely address the actual ways in which social factors directly affect variation in signaling. Indeed, the underlying mechanisms of this link are usually left unexplored, failing to uncover the specific attribute of communication that would be co-evolving with specific aspects of sociality. I, therefore, make a plea for expanding tests of the SCHCC in 1) scope (systematic approach across modalities) and 2) depth (characterization of the observed relationships) as I believe it may significantly advance our understanding of the intricate links between animal sociality and communication. To address point 1), I offer in chapter II a comprehensive approach of the cross-modal communicative systems of two closely related true lemur species having similar morphology, living in similar habitats, but differing in their social systems. I studied wild Eulemur rufifrons and E. mongoz in Madagascar, respectively in Kirindy and Ankatsabe forests for 12 months. I describe a new analytical framework to assess the complexity of signaling systems across modalities. Applying a multimodal approach may help to uncover the different selective pressures acting on the communicative system and to understand better adaptive functions that might be unclear from the study of its separate components independently. E. rufifrons, the species having the more complex social system, also had overall a more complex communicative system than the one of the E. mongoz. Both careful choices of the species to compare to limit the effect of possible additional selective pressures and exploration of the social function of the non-homologous signals allow concluding that this increased complexity of the communicative system in E. rufifrons is most likely associated with social selective pressures. I developed this new analytical framework, partly based on using a cross-modal network approach, with the perspective of facilitating cross-taxonomic comparisons. Moreover, this approach may be combined with new multi-dimensional approaches of social complexity and contribute to a more holistic approach to the tests of the SCHCC. By this, we should be able to derive new testable hypotheses that would contribute to better understand the course of events that have led to the evolution of communication diversity in its distinct dimensions. In chapter III, I address point 2) by investigating the impacts of sociality on the expression of a multimodal signal, the anogenital scent-marking behavior in wild red-fronted lemurs. I specifically investigated intragroup audience effects on anogenital scent-marking behaviors in a wild population of red-fronted lemurs and particularly whether males and females differed in this aspect and if these differences may reveal functional differences associated with anogenital scent-marking across sexes. I found an intragroup audience effect in males but not in females. Males deposited less often anogenital marks when more males were present within a three meters range compared to five- or ten-meters ranges. Males may prefer to reduce the risk of physical contact by avoiding to scent-mark near other males, and/or give priority to other males to scent-mark. With these results, I provide important insights into the functional significance of anogenital scent-marking in red-fronted lemurs and support the idea of greater intragroup social pressures associated with anogenital scent-marking in males than in females in egalitarian species. Studying the flexibility of complex signal usage (e.g., occurrence or structural modifications) across social contexts (audiences) should permit the identification of different individual social characteristics that may elicit or constrain complex signal expression. These social characteristics may later constitute social pressures acting for or against the evolution of these complex signaling behaviors. In chapters IV and V, I also address ethical questions related to this project and the way I tried to adapt and best address my responsibilities for animal welfare. In chapter IV, I expose some technical details and ethical concerns experienced during the choice of my field sites. While in chapter V (Buil and Peckre et al. 2019) I present a remote releasable collar system developed in collaboration with the Neurobiology Laboratory (German Primate Center, Göttingen, Germany) intending to provide a tool to significantly reduce the number of captures in studies using bio-logging for medium-sized mammal species. Overall, by emphasizing the importance of the multimodal nature of communicative systems and the social context in which signals are exchanged, I hope to stimulate the development of new tests of the SCHCC based on this expanded framework. I additionally argue for the importance of looking across research fields since striking parallels may be observed between animal behavior and linguistic research when addressing the origins of communication complexity, be it in the form of human language or animal signaling.
... Minimum observed age at first conception in females was taken from the literature (Anderson and Simpson, 1979;Coe et al., 1979;Geissmann, 1991;Zehr et al., 2014Zehr et al., , 2019 and is used as a proxy for age at maturity, which should generally correspond to overall pace of development. Age at first conception is strongly correlated with body mass (ln age vs. ln body mass, R 2 ¼ 0.824), so ln age was regressed against ln body mass and the residuals were used for subsequent analyses. ...
... The caper package implements Freckleton et al.'s (2002) PGLS method. All nonhuman primate observations of age at first conception were carried out on captive populations of primates, for which ages are frequently known and reproductive status is easier to track, but captive individuals probably mature more quickly than individuals in the wild (Geissmann, 1991;Wallis, 1997;Reichard and Barelli, 2008;Zehr et al., 2014). Only captive values were used here to control for this variation between wild and captive populations. ...
Recent studies on hominin craniofacial evolution have focused on phenotypic integration or covariation among traits. Covariation is thought to significantly affect evolutionary trajectories, shaping the ways in which hominins and other primates could have evolved. However, the ways in which covariation itself evolves are not well understood. This study aims to investigate the role of phylogeny, development, body size, and positional behavior in shaping the strength of covariation in strepsirrhine and catarrhine primate crania (n ¼ 1009, representing 11 genera). These factors may have been catalysts for change in the magnitude of covariation, and they have changed significantly during primate evolution and particularly hominin evolution. Modern humans in particular have slow developmental trajectories, large bodies, and a unique form of locomotion in the form of orthograde bipedalism. Variance of eigenvalues, mean integration, mean evolvability, and mean conditional evolvability was estimated and their relationship to the various factors described earlier was assessed using phylogenetic and nonphylogenetic analyses. Results indicate that some phylogenetic signal is present, but it is not equivalent across integration statistics or cranial regions. In particular, these results suggest that closely related species are more similar than more distantly related species in evolvability of the cranial base and integration of the face. Two divergent patterns were also identified, in which covariation and evolvability of the cranial base are linked to developmental rate, but those of the face are linked to body size. Neither locomotion nor posture appears related to covariation or evolvability of the primate cranium. These results suggest that overall low covariation observed in the hominin cranium may be a result of separate trends in different cranial regions.
... Fifteen primates, two fruit bats (Rousettus leschenaulti), and one tree shrew (Tupaia belangeri) were studied; specimens at multiple ages were available for some primate genera and the fruit bat (Table 1). In most cases, age in days was known based on the records of the Duke Lemur Center (DLC, Zehr et al., 2014). Some DLC specimens for which "0 days" of age was recorded were examined and categorized as fetal based on dental maturation and external features (see Smith et al., 2015, Smith, Curtis, & KP Bhatnagar, 2020 for further details). ...
Living primates show a complex trend in reduction of nasal cavity spaces and structures due to moderate to severe constraint on interorbital breadth. Here we describe the ontogeny of the posterior end of the primate cartilaginous nasal capsule, the thimble shaped posterior nasal cupula (PNC), which surrounds the hind end of the olfactory region. We used a histologically sectioned sample of strepsirrhine primates and two non‐primates (Tupaia belangeri, Rousettus leschenaulti), and histochemical and immunohistochemical methods to study the PNC in a perinatal sample. At birth, most strepsirrhines possess only fragments of PNC, and these lack a perichondrium. Fetal specimens of several species reveal a more complete PNC, but the cartilage exhibits uneven or weak reactivity to type II collagen antibodies. Moreover, there is relatively less matrix than in the septal cartilage, resulting in clustering of chondrocytes, some of which are in direct contact with adjacent connective tissues. In one primate (Varecia spp.) and both non‐primates, the PNC has a perichondrium at birth. In older, infant Varecia and Rousettus, the perichondrium of the PNC is absent, and PNC fragmentation at its posterior pole has occurred in the former. Loss of the perichondrium for the PNC appears to precede resorption of the posterior end of the nasal capsule. These results suggest that the consolidation of the basicranial and facial skeletons happens ontogenetically earlier in primates than other mammals. We hypothesize that early loss of cartilage at the sphenoethmoidal articulation limits chondral mechanisms for nasal complexity, such as interstitial expansion or endochondral ossification.
