Thesis (Ph.D.) - University of St Andrews, November 2009. / Restricted until 5th November 2011.

Thesis advisor: David Krauss / Behavior in a confined group of mandrills (Mandrillus sphinx) and a confined group of ring tailed lemurs (Lemur catta) were analyzed to reveal any significant differences in agonistic behaviors and to assess the varying stress levels between individuals. I predicted that the activity rate of the individuals would determine the amount of agonistic behavior demonstrated, specifically that more active individuals would be more frequently performing agonistic behaviors than those who were less active. The mandrills as a whole exhibited a higher activity rate than the lemurs, and the proportion of time spent exhibiting agonistic behaviors was also higher, as expected. These results suggest that the mandrill population is under more stress than the lemurs. Differences in the age makeup of these groups may partially explain the behavioral differences that occurred: the mandrills' group included a juvenile who was considerably more active than his parents while all three lemurs observed were adults. Differences in the size of the exhibit may also explain the differences as the exhibit for the mandrills was smaller than that of the lemurs, while the mandrills were more than triple the lemurs' size. This analysis supports earlier studies: that primate behavior is influenced strongly by their environment and its cohabitants. / Thesis (BS) — Boston College, 2004. / Submitted to: Boston College. College of Arts and Sciences. / Discipline: Biology. / Discipline: College Honors Program.

Madagascar’s lemurs are the most endangered group of mammals in the world, with 94% of species threatened with extinction. Forest loss is one the greatest threat to these arboreal primates, but hunting, habitat degradation, and climate change also threaten their survival. Lemurs are a diverse group of more than 100 species; and their ecological traits shape how species respond to anthropogenic pressure. Incorporating knowledge of species’ ecological niches and evolutionary histories can contextualize threats and improve conservation assessments. In this dissertation, I investigate what constitutes suitable habitat for lemurs in light of the threats present, their sensitivity to forest fragmentation, their dispersal ability, and their ecological uniqueness. I obtained data about lemur distributions in two ways. First, I conducted field surveys of the Critically Endangered blue-eyed black lemur (Eulemur flavifrons), which only occurs in the ecotone between eastern rainforest and western dry forest in the Sahamalaza region. I also surveyed the range of sister species, the black lemur (E. macaco), which inhabits nearby eastern rainforest in the Manogarivo region. I focused on areas that have not been surveyed recently and on the poorly studied boundary between the species to collect observations from the breadth of these species’ ecological ranges. I also documented threats, including incursions into protected areas, and collected fecal samples to test whether whole genomes could be obtained noninvasively for analyses of local adaptation in these species. Second, I searched online databases and published literature for GPS localities for all species of lemur. I used these records, along with the ones collected in the field, to construct ecological niche models for nearly all species of lemur using Maxent. For the blue-eyed black lemur and the black lemur, I estimated the remaining area they can occupy based on these models and the threat survey data. Next, I examined the role of not just forest loss, but forest degradation, in determining where lemur species occur. I used high-resolution forest cover maps to determine lemurs’ tolerance for characteristics of degraded forest, including distance to the edge and mean patch size. I then limited species niche model to only intact, forested habitat. Lastly, using the sportive lemurs (genus Lepilemur) as an example, I evaluate how the inability to disperse across large rivers has influenced ecological niche diversity. I also examine what limited dispersal ability will mean for these species as climate change causes their ranges to shift. Field surveys in the Sahamalaza and Manongarivo regions revealed extensive threats to blue-eyed black lemurs, from traps to cattle incursions and fire. I found no evidence of sympatry, but did locate an undocumented population of E. flavifrons north of the Andranomalaza River. Madagascar National Parks (MNP) managed protected areas appear to have less human incursion than NGO-managed protected areas. Further investigation of the ecological distinctiveness of these species is possible via non-invasive methods: I sequenced whole genomes at 2.3x coverage from eight of the fecal samples collected during this study. While SNPs indicating a loss of function did not reveal any patterns, sequencing additional samples could make studies of local adaptation and population genetic diversity possible. At the regional scale, forest conversion is a grave threat to lemurs. When forest loss and degradation are considered in habitat models, lemur species have lost 51% of their habitat in the last 30 years. Proximity to a forest edge rendered more forested areas too degraded for lemurs than did mean patch size. This result is likely the influence of human contact nearer the forest edge. I recommend urgent support for reserves like Beanka, Tsimembo Forest, Ranobe PK 32, and Amoron’i Onilahy, which have highly suitable, intact forest for many lemur species. Spaces like these will be important for conserving the remarkable diversity within the sportive lemur clade. Though their distribution is largely explained by riverine barriers, I show a role for ecological niche divergence and local adaptation in accelerating allopatric speciation. These same rivers will limit their ability to track climatically suitable areas as climate change progresses: sportive lemurs as a group will lose nearly a quarter of their accessible habitat to climate change by the 2070s. While my results are focused on the particulars of lemur conservation in Madagascar, the methods I have presented here are broadly applicable to other threatened species. Piggybacking fecal sample collection onto rapid field surveys is straightforward. The possibility of obtaining whole genomes from non-invasive samples presents a new way to answer questions about local adaptation without risking injury to other arboreal study subjects, like Neotropical monkeys, or for elusive species like big cats. For threatened species, their climatic niche only dictates part of their distribution. The habitat quantification pipeline presented here takes advantage of thirty-five years of research in Madagascar to estimate species’ tolerance for forest fragmentation. While these records are impressive for primates, they are dwarfed by those available for passerines, through scientific literature and online repositories like eBird. By integrating field surveys, ecological niche modeling, and non-invasive genomics, we can begin to understand the complex threats facing species like lemurs and the options for ensuring their survival.

All living hominoids are characterized by taillessness and adaptations to orthograde (upright) trunk posture. Accordingly, these features have importance for our understanding of ape origins, evolutionary relationships and positional behaviors. Despite extensive study of the hominoid postcranial skeleton, researchers continue to face difficulty identifying taillessness and orthogrady from fossil material. In part, difficulties persist because although the Miocene fossil record indicates that the evolution of tail loss and orthogrady was decoupled, previous research has focused primarily on how the skeletal anatomy of extinct apes resembles that of living apes, in which these traits appear in conjunction. The remarkable diversity in tail lengths and positional behaviors exhibited by other mammals presents a valuable opportunity to employ the strength of the comparative method for testing functional hypotheses. The goal of this dissertation is to identify anatomical correlates of tail length and positional behaviors from sacral and caudal vertebral morphology among primates and other mammals in three studies. The first study examines the relationship between trabecular structure in the first sacral vertebra and positional behaviors (N= 78 primates). The second study quantifies aspects of internal (N=78 primates) and external (N= 472 mammals) sacral anatomy for correlates of relative tail length. The third study evaluates the functional morphology of caudal vertebrae among nonprehensile-tailed primates and other mammals that vary in relative tail length, offering additional insight into the anatomy associated with tail loss (N=333). The relationship between trabecular structure in the proximal sacrum and positional behaviors among living primates is somewhat unclear. Some trabecular parameters in the distal sacrum appear to have a relationship with tail length. Results support the functional links between previously and newly defined metrics from the external morphology of sacra and caudal vertebrae, and relative tail length, among primates and other mammals. Identified anatomical correlates from the extant primate sample are used to reconstruct the tail lengths of extinct primates. From the sacral data, Proconsul is reconstructed as tailless, Archaeolemur likely possessed a long tail, and Palaeopropithecus, Megaladapis and Epipliopithecus had short tails. From the caudal vertebrae data, Archaeolemur is reconstructed as possessing a long tail and Palaeopropithecus is reconstructed as having a short tail. / text

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Long isolation and the island environment of Madagascar has led to the evolution of a number of unusual traits in the Lemuriformes, including reproductive synchrony, sexual monomorphism, female dominance, and female feeding priority. Though gestation and lactation are costly in all mammals, the unpredictable and often harsh environment of Madagascar may have led to the selection of particular adaptive traits which offset some of the high costs of reproduction in female lemurs. Sex differences in feeding behavior between male and female Lemur catta, which have been documented previously may he a reflection of increased reproductive female nutritional need, although differences in actual nutritional intake has not been examined. In August and September of 2005 I collected 217 hours of focal feeding data on 9 male and 9 gestating female L. catta from two social groups. at the Beza Mahafaly Special Reserve in southwestern Madagascar. Additionally, I collected representative samples of all plant foods eaten by the focal animals. Since reproductive females have higher metabolic needs, I predicted that when compared to males, gestating females would consume more, feed for longer periods, and ingest higher relative amounts of crude protein and minerals. and lower relative amounts of fiber. Additionally, since the two focal social groups have similar and over-lapping home ranges, I predicted that no feeding differences (amount consumed. time spent feeding, ingestion of crude protein, minerals and fiber) would be present between social groups. I found no statistically significant differences in feeding behavior between males and females. while nutritional sex differences were limited to females consuming increased phosphorus (P= 0.004) and potassium (P=0.015 ). Furthermore, although I detected no between group differences nutrient consumption or amount of food consumption Green Group did spend significantly more time foraging, when compared to Red Group (P=0.004). These data may be explained by the prior activity of cyclone Ernest. which greatly reduced food availability and caused a fruiting failure of Tamarindus indica, a keystone resource of gallery forest L. catta. Additionally, although both focal groups ventured outside of the forest to forage on agricultural or introduced plant species. Green Group only fed on crop foods on one occasion. while Red Group fed daily on the easily processed crop foods, which may have decreased their foraging time. Ability to exploit novel resources and adapt to environmental extremes may be a key feature enabling L. catta to persist alongside humans in the harsh environment of Madagascar.

The origin and geographical distribution of mammalian species (my examples are lemurs and bats) correlate with predictable chromosomal structural changes (KFT=karyotypic fission theory). Chromosome studies provide information about fertility between individuals and they are significant for identification of the geographical origin of reproductive isolation within mammal families. Each family predictably has chromosome sets with numbers that range from one to double the lowest number of chromosomes. The chromosome numbers of all species within a single family are used to reconstruct that family’s evolutionary geographical dispersion. Polymorphic chromosome numbers (that is a range such as 34, 35, 36, 37, and 38) in a single population indicate the location where chromosomal diversification arose. Chromosome numbers of descending order correlate with relative distance from fission epicenters as the fissioned chromosomes gradually spread to neighboring populations. Furthermore, the location of chromosomal diversification (that is “karyotypic fission events) is associated with geographical “zones of transition” (after Professor R.W. Wilkie). My analysis, mapped one (Lepilemuridae) of the five families of lemurs (Class Mammalia, Order Primates, sub-order Lemuridae). The origin of this family’s diversification is here hypothesized to have occurred at an ecological transition zone in Northern Madagascar between a humid evergreen-forest that extends to the East relative to a dry deciduous forest along the West Coast. My analysis of Vespertilionidae (insectivorous bats representing one third of all bat species) suggests a diversification event occurred in Asia; South China. Geographical distribution is important in the formation of biological diversity. A single species can inhabit a wide range and exhibit great diversity that is brought about by natural selection. The Holarctic reindeer found in Scandinavia, Russia, China, Canada and Alaska (including caribou) are all a single species Rangifertarandus that exhibits variation in size and in coat pattern, changes brought about by adaptive selection by the environment or human selective breeding but they all have 70 similar chromosomes and they are all reproductively compatible. There is a single species of reindeer. Although, there is measurable DNA sequence divergence; there has been no “speciation” as these circumpolar cervids are genetically compatible.

This dissertation investigates reproductive schedules of brown mouse lemurs at Ranomafana, using intensive trapping techniques. The reproductive condition of female mouse lemurs was recorded on the basis of vaginal morphology, vaginal smears, body mass gain profiles and nipple development. Testis size was measured in males throughout the reproductive season. The timing of the first seasonal estrus was determined in frequently captured females over multiple years and it showed individual periodicities close to 365 days, consistent with endogenous regulation and entrainment by photoperiod. The timing of estrus did not correlate with female age or body mass. Males showed testicular regression during the rainy season, although there was high inter-individual variation in testes size at any given point during the reproductive season. Furthermore, some individuals completed testicular regression earlier than others. Implications for polyestry are discussed. For comparative purposes, mouse lemurs were also trapped at two study sites in the Tsinjoarivo area: one in a forest fragment and the other within continuous forest. These forests are higher in altitude than the main study area at Ranomafana. Trapping success for mouse lemurs was lower at Tsinjoarivo than Ranomafana. Albeit preliminary, data from Tsinjoarivo suggest that females have lower reproductive success than do females at Ranomafana. Nevertheless, mouse lemurs in the Tsinjoarivo forest fragment did not appear to be in "poorer" condition than those in the continuous forest. It had been reported in the literature that western gray mouse lemurs captured in secondary forests have lower body masses and lower recapture rates than those captured in primary forest; in fact, the opposite was true of the mouse lemurs at Tsinjoarivo. I additionally collected data on a larger member of the family Cheirogaleidae, the dwarf lemurs (Cheirogaleus), which live in sympatry with Microcebus at Ranomafana and Tsinjoarivo. I analyzed the patterns of growth, development and reproduction in Cheirogaleus and Microcebus and compared dwarf and mouse lemurs to other similarly-sized prosimians which do not undergo torpor or hibernation. These comparisons draw attention to the unusual reproductive and metabolic strategies employed by cheirogaleids to cope with Madagascar's unpredictable environments, which ultimately define their very unique life histories.

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By studying how captive animals use outdoor space, we can determine which areas fulfill their biological and behavioral needs to improve enclosure design for animal welfare and visitor experience. The aim of the study was to determine the differential use of outdoor space in a mixed exhibit of captive ring-tailed lemurs (Lemur catta) and red ruffed lemurs (Varecia rubra), and to assess both the effect of adding environmental enrichment and possible visitor and meteorological effects on the lemurs’ use of space and behavior. For one month, five-minute interval scan sampling was used to record lemur location and behavior, as well as the meteorological conditions and presence of zoo visitors in the lemurs’ outdoor enclosure. That baseline was followed by four alternating two-week periods of food or structural enrichment, both with and without visitors. Enrichment increased the lemurs’ use of the enriched sectors, decreased resting, and increased locomotion. Structural enrichment increased their exploratory behaviors and stimulated arboreal locomotion. Both species preferred sunny and warm conditions for sunbathing and resting, while moving more around the enclosure in cooler and cloudier weather. The visitor effect on the lemurs’ use of space was weaker than the effects of enrichment and meteorological conditions. The availability of areas to hide and possible habituation to humans may have played a role in the reduced visitor effect. The results of the study showed inter-specific differences in the lemurs’ use of space and behavior and a complex combined effect of enrichment, visitor presence and meteorological conditions.