Motivations for the Ownership of Captive Lemurs in Madagascar

The live capture of primates is occurring throughout the tropics and can be a threat to their conservation. Primates are owned as pets for a variety of reasons. Studies of the motivations for primate ownership have been conducted in several countries where they are endemic, but no study has examined this issue in Madagascar. Madagascar is home to the highest number of threatened primate taxa in any one country, and an estimated 28,000 lemurs were kept in illegal captivity from 2010 to mid-2013. We aimed to expand knowledge about the motivations of lemur ownership in Madagascar. Data were collected via a web-based survey (n = 229 respondents) and from the websites and social media pages of 25 hotels. We found that many lemurs (45%) were seen on the premises of a business or in a private home (27%). Many lemurs were perceived to be kept as personal pets (37%) or for money-making or tourism purposes (20%). When lemurs were used for money-making, owners could receive indirect (72% of the time) and direct benefits (28%). Hotels showing photographs of captive lemurs on their websites and social media sites charged USD 25.69 more per night for a standard room than hotels that did not show such photographs. We found little evidence that captive lemurs are kept as a social status symbol, for captive breeding, or as a fallback food. These findings provide evidence that the motivations for the ownership of, usually illegal, captive lemurs is typically linked with money-making or with the desire to have a lemur as a pet. These data can help target new outreach programs.     

Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers

Aim Elucidation of the influence of river systems on the distribution of lemurs. Location Humid forests of Madagascar. Methods We review the elevational distribution of Malagasy lemurs to address hypotheses of the role of rivers as physical barriers. Main conclusions Rivers are barriers for some species. However, several lemurs have altitudinal ranges that are higher than the headwaters of a given river, and in such cases these species are able to disperse across the source.     

Origins,Diversity and Relationships of Lemurs

I review new evidence on origins and adaptive radiation of Malagasy lemurs, a remarkably diverse group containing 13% of living primate species. The number of recognized lemur species has increased significantly, partly due to research revealing specific subdivisions within known populations but mainly because of discovery of new populations through fieldwork. Some species feared to be extinct have also been rediscovered. Specific numbers have increased particularly in small-bodied, cryptic genera for which continued research will surely reveal even more species.Adaptative radiation of lemurs has been essentially confined to Madagascar. The high density of lemur species on that island, associated with very small geographical ranges, has major implications both for their evolutionary divergence and for conservation. Reconstructions of phylogenetic relationships among primates have been considerably enhanced by DNA sequence data. Sufficient data are now available from both nuclear and mitochondrial sequences to examine relationships among and within the major groups of living primates. Most studies have confirmed that lemurs constitute a monophyletic sister-group of the lorisiform clade and all exclude a specific relationship between cheirogaleids and lorisiforms repeatedly inferred from morphological evidence. However, some analyses indicate that the aye-aye may have branched away before the divergence between other lemurs and lorisiforms. DNA sequence analyses have also yielded a broad consensus for relationships between Eulemur, Hapalemur, Lemur and Varecia: Varecia branched away first, while Lemur is more closely related to Hapalemur than to Eulemur. As debate about phylogenetic relationships among lemurs and other primates seems to have been settled in favor of lemur monophyly (possibly excluding the aye-aye), only a single invasion of Madagascar is required; but it must still be explained how ancestral lemurs could have migrated there at an appropriate time. Separation between Madagascar and Africa was apparently complete by about 120 Ma, too far in the past for direct overland migration. A recent hypothesis suggested that uplifted land in the Mozambique Channel assisted colonization of Madagascar 26-45 Ma, seemingly agreeing with an estimated date of about 40 Ma for divergence of lemurs from other primates. However, mounting evidence suggests that divergence occurred significantly earlier. Because the earliest known fossil representatives of several modern orders of placental mammals (including primates) are dated no earlier than the early Tertiary, it is widely accepted that their divergence took place after the Cretaceous/Tertiary mass extinction. Yet the known fossil record can only yield minimum divergence times; if sampling is poor and/or biased there may be a considerable discrepancy between minimum and actual dates. There is, for example, virtually no known fossil record for lemurs in Madagascar and the earliest known representatives are subfossil lemurs, so in this case a direct reading of the fossil record would indicate that the lemurs first originated just a few thousand years ago! Examination of underestimation of times of origin because of poor sampling in the fossil record has confirmed previous suggestions that primates originated considerably earlier than generally believed. Several recent phylogenetic reconstructions based on DNA sequence data and using calibration dates derived from groups other than primates provide independent support for this inference. Overall, it now seems that primates originated at around 90 Ma rather than the 55 Ma indicated by direct reading of the known fossil record. Hence, colonization of Madagascar by lemurs would have taken place at about 80 Ma, double the date usually accepted, and should be interpreted in terms of contemporary continental relationships.     

Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ring-tailed lemurs in southwestern Madagascar

The ring-tailed lemur (Lemur catta) is an endangered species found in southwestern Madagascar, and understanding infectious disease susceptibility is an essential step towards the preservation of wild and captive lemur populations. Lemurs are primates that are widely dispersed throughout the island of Madagascar and may serve as hosts or reservoirs for zoonotic infections. The aim of this study was to determine the prevalence of antibodies to West Nile virus (WNV), simian immunodeficiency virus (SIV), and herpes simplex virus type 1 (HSV-1) in a population of free-ranging ring-tailed lemur from the Beza Mahafaly Special Reserve, Madagascar. Samples were collected from 50 animals during field capture studies in June and July 2004 and assayed for presence of viral antibodies during the 12 mo following collection. Forty-seven of the 50 lemurs sampled had antibodies against WNV detectable by epitope-blocking enzyme-linked immunosorbent assay (ELISA). In addition, 50 of 50 samples had titers against WNV ranging from 80 to > or = 1,280 using plaque reduction neutralization test (PRNT(90)). Ten lemurs had antibodies against lentiviral antigens as determined by Western blot analysis. None of the lemurs had antibodies against HSV-1 using ELISA.     

Use of Mangroves by Lemurs

Despite an increasing recognition of the ecosystem services provided by mangroves, we know little about their role in maintaining terrestrial biodiversity, including primates. Madagascar’s lemurs are a top global conservation priority, with 94 % of species threatened with extinction, but records of their occurrence in mangroves are scarce. I used a mixed-methods approach to collect published and unpublished observations of lemurs in mangroves: I carried out a systematic literature search and supplemented this with a targeted information request to 1243 researchers, conservation and tourism professionals, and others who may have visited mangroves in Madagascar. I found references to, or observations of, at least 23 species in 5 families using mangroves, representing >20% of lemur species and >50% of species whose distributions include mangrove areas. Lemurs used mangroves for foraging, sleeping, and traveling between terrestrial forest patches, and some were observed as much as 3 km from the nearest permanently dry land. However, most records were anecdotal and thus tell us little about lemur ecology in this habitat. Mangroves are more widely used by lemurs than has previously been recognized and merit greater attention from primate researchers and conservationists in Madagascar.     

Evidence of early butchery of giant lemurs in Madagascar

We report here definitive evidence of butchery, most probably associated with hunting, of giant extinct lemurs by early human settlers in Madagascar. Specimens of Palaeopropithecus ingens and Pachylemur insignis from two sites in southwestern Madagascar, Taolambiby and Tsirave, show classic signs of butchering. We compared these to the bones (also from Taolambiby) of butchered Propithecus verreauxi, a lemur still living in the region. The characteristics of the tool-induced extinct-lemur bone alterations (sharp cuts and chop marks near joints, oblique cuts along the shafts, spiral fractures, and percussion striae) suggest skinning, disarticulation, and filleting. Conclusive evidence of megafaunal modification by humans in Madagascar was limited previously to a few hippo and elephant bird bones and one extinct aye-aye tooth. New evidence comes not from archaeological sites, but from specimens collected in the early 1900s, without stratigraphic records, at "subfossil" sites (i.e., sites renowned for their late Pleistocene or Holocene fossils, often lacking human artifacts). Whereas these are hardly the most ideal samples for analysis of this kind, careful scrutiny of the characteristics of the cut marks has allowed us to document butchery beyond any reasonable doubt. One bone with definitive cut marks has been dated to the very earliest part of the human period in Madagascar. Continued, careful research on the bones in subfossil collections is warranted.     

Conservation biology of Malagasy strepsirhines: a phylogenetic approach

The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis, Allocebus trichotis, Lepilemur septentrionalis, Indri indri, and Mirza coquereli. Regional conservation priorities are highest for lemurs that range into northeast humid forests and western dry forests. Expansion of existing protected areas in these regions may provide the most rapid method for preserving lemurs. In the long term, new protected areas must be created because there are lemur species that: 1) are not found in existing protected areas, 2) exist only in one or two protected areas, and 3) are still being discovered outside the current network of protected areas. Data on the population dynamics and feeding ecology of phylogenetically important species are needed to ensure that protected areas adequately conserve lemur populations in Madagascar.     

The extinct sloth lemurs of Madagascar

Paleontological expeditions to Madagascar over the past two decades have yielded large quantities of bones of extinct lemurs. These include abundant postcranial and cranial remains of new species belonging to a group of giant extinct lemurs that we have called sloth lemurs due to their remarkable postcranial convergence with arboreal sloths. New fossils have come from a variety of locations in Madagascar, including caves in the Northwest (Anjohibe) and the Ankarana Massif, located in the extreme north, as well as pits in the karstic plains near Toliara in southwestern Madagascar. The most spectacular of these is the extremely deep pit (>100 m) called Ankilitelo, the “place of the three kily trees.” These new materials provide insights into the adaptive diversity and evolution of sloth lemurs. New carpal and pedal bones, as well as vertebrae and other portions of the axial skeletons, allow better reconstruction of the positional behavior of these animals. New analytical tools have begun to unlock the secrets of life‐history adaptations of the Palaeopropithecidae, making explicit exactly what they had in common with their relatives, the Indriidae. Paleoecological research has elucidated the contexts in which they lived and the likely causes of their disappearance.     

Extinction and ecological retreat in a community of primates

The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced community-wide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.     

Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar

Hybrid zones in ecotones can be useful model systems for the study of evolutionary processes that shape the distribution and discreteness of species. Such studies could be important for an improved understanding of the complex biogeography of Madagascar, which is renowned for its outstanding degree of small-scale endemism. Certain forest remnants in central Madagascar indicate that transitional corridors across the island could have connected microendemics in different forest types in the past. Evolutionary processes in such corridors are difficult to study because most of these corridors have disappeared due to deforestation in central Madagascar. We studied a hybrid zone in one of the few remaining ecotonal corridors between dry and humid forests in Madagascar, which connects two species of mouse lemurs, Microcebus griseorufus in dry spiny forest and Microcebus murinus in humid littoral forest. We sampled 162 mouse lemurs at nine sites across this boundary. Morphometric analyses revealed intermediate morphotypes of many individuals in transitional habitat. Bayesian clustering of microsatellite genotypes and assignment tests yielded evidence for a mixed ancestry of mouse lemurs in the ecotone, where we also observed significant linkage disequilibria and heterozygote deficiency. In contrast to these observations, mitochondrial haplotypes displayed a sharply delimited boundary at the eastern edge of spiny forest, which was noncoincident with the signals from microsatellite data. Among several alternative scenarios, we propose asymmetric nuclear introgression due to male-biased dispersal, divergent environmental selection, and an expansion of dry spiny forest in the course of aridification as a probable explanation of our observations.     

Complementary approaches of cytogenetics and molecular biology to the taxonomy and study of speciation processes in lemurs

The lemurs, prosimian primates of Madagascar, constitute a zoological group containing numerous species and subspecies. Their taxonomy remains controversial. Depending on the authors and the techniques they have used, the number of species varies between 39 and 52. In addition, although a monophyletic origin of the settlement of Madagascar is the most commonly held opinion, recent studies based on molecular biology do not exclude two independent colonization events, one involving Daubentonia and a second giving rise to the other lemurs. 1 .     

Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes

Madagascar harbors four large adaptive radiations of endemic terrestrial mammals: lemurs, tenrecs, carnivorans, and rodents. These rank among the most spectacular examples of evolutionary diversification, but their monophyly and origins are debated. The lack of Tertiary fossils from Madagascar leaves molecular studies as most promising to solve these controversies. We provide a simultaneous reconstruction of phylogeny and age of the four radiations based on a 3.5-kb data set from three nuclear genes (ADRA2B, vWF, and AR). The analysis supports each as a monophyletic clade, sister to African taxa, and thereby identifies four events of colonization out of Africa. To infer the time windows for colonization, we take into account both the divergence from the closest non-insular sister group and the initial intra-insular radiation, which is a novel but conservative approach in studies of the colonization history of Madagascar. We estimate that lemurs colonized Madagascar between 60 million years ago (Mya) (split from lorises) and 50 Mya (lemur radiation) (70-41 Mya taking 95% credibility intervals into account), tenrecs between 42 and 25 Mya (50-20 Mya), carnivorans between 26 and 19 Mya (33-14 Mya), and rodents between 24 and 20 Mya (30-15 Mya). These datings suggest at least two asynchronous colonization events: by lemurs in the Late Cretaceous-Middle Eocene, and by carnivorans and rodents in the Early Oligocene-Early Miocene. The colonization by tenrecs may have taken place simultaneously with either of these two events, or in a third event in the Late Eocene-Oligocene. Colonization by at least lemurs, rodents, and carnivorans appears to have occurred by overseas rafting rather than via a land bridge hypothesized to have existed between 45 and 26 Mya, but the second scenario cannot be ruled out if credibility intervals are taken into account.     

The enigma of antipredator behavior in lemurs: Evidence of a large extinct eagle on Madagascar

Numerous zoologists who study diurnal lemurs on Madagascar have noted that they react strongly to the presence of birds of prey. For two of the most intensively studied lemurs, Propithecus verreauxiand Lemur catta,there are few documented cases of raptor predation. Thus, the maintenance of this stereotypic response is enigmatic. Bird bones recovered from cave surface deposits in southwestern Madagascar include the remains of an eagle (Aquila),a genus that has disappeared from Madagascar and that would have been capable of hunting animals the size of adult P. verreauxi and L. catta.The stereotypic response of these two lemurs toward raptors may have been retained from the period when this extinct eagle inhabited the island and is reinforced by rare acts of predation by extant birds of prey.     

Social Organization of Lepilemur ruficaudatus

We characterize the spatial organization of red-tailed sportive lemurs (Lepilemur ruficaudatus) as a key aspect of their social organization and social system. Sportive lemurs are small (<1000 g), nocturnal and folivorous primates endemic to Madagascar. We studied a population of 57 individually-marked individuals in Kirindy Forest, western Madagascar, between 1995 and 2001. We radio-tracked 20 males and 26 females of the marked population to obtain detailed information on the size and location of their home ranges. Census data and morphometric measurements provided complementary data sets. Males and females occupied small (<1 ha) home-ranges. Long-term records from 9 individuals revealed home-range stability over several years. In 4 cases home ranges overlapped extensively with that of one member of the opposite sex; in 2 cases, a spatial association of 1 male and 2 females occurred. However, home ranges overlapped very little with neighboring individuals of both sexes. During the study period, spatially associated individuals used on average 5.6 sleeping trees within 117 days, but they spent on average only about every fourth night together. The data suggest that home ranges in red-tailed sportive lemurs are exclusively used by pairs or trios and that the modal social organization of red-tailed sportive lemurs is pair-living.     

DNA from extinct giant lemurs links archaeolemurids to extant indriids

Background  

Although today 15% of living primates are endemic to Madagascar, their diversity was even greater in the recent past since dozens of extinct species have been recovered from Holocene excavation sites. Among them were the so-called "giant lemurs" some of which weighed up to 160 kg. Although extensively studied, the phylogenetic relationships between extinct and extant lemurs are still difficult to decipher, mainly due to morphological specializations that reflect ecology more than phylogeny, resulting in rampant homoplasy.     

Surveys of sympatric lemurs at Anjamena, north-west Madagascar

In order to assess the status of lemurs along the lower reaches of the Mahavavy in north-west Madagascar, we carried out transect line sampling at Anjamena between April and August 1995. These data were complemented by additional absence–presence surveys conducted in 1994 and 1995 in many of the remaining forested areas of the region. This is the first study of lemur population density estimates for the faunal subregion between the rivers Mahavavy and Betisboka. Six sympatric lemurs are found at Anjamena: Cheirogaleus medius, Eulemur fulvus rufus, E. mongoz, Lepilemur sp., Microcebus murinus and Propithecus verreauxi coronatus. Data suggest that in some parts of the region large numbers of lemurs may still be found (E. f. rufus 121 individuals per km², E. mongoz (45), Lepilemur sp. (110), M. murinus (85) and P. v. coronatus (173)). No density data are provided for C. medius. In conclusion, as high lemur population densities may still be found and, in particular, P. v. coronatus is not known to exist in any protected area, Anjamena could serve as an important addition to the protected area system of north-west Madagascar.     

The Use of Vanilla Plantations by Lemurs: Encouraging Findings for both Lemur Conservation and Sustainable Agroforestry in the Sava Region,Northeast Madagascar

Extensive areas of forest are cleared every year to establish new agricultural land in the tropics, resulting in a catastrophic loss in habitat for the world’s primates. A prominent example of this process is Madagascar, where an increasing demand for arable land has led to the once-forested landscape to be now dominated by agricultural areas used for the cultivation of food and cash crops. Despite the prominence of these plantations throughout Madagascar, their suitability as a habitat to support endemic lemur populations remains unclear. Here, we assessed lemur presence in vanilla plantations, Madagascar’s principal export crop, within the northeastern Sava region with the use of line transects. We confirmed the presence of five lemur species, four of which were nocturnal cheirogaleids, in these vanilla plantations. Intensively farmed vanilla plantations and those in existing stands of vegetation supported at least one species of lemur. Furthermore, lemurs were significantly more likely to be present in plantations grown close or adjacent to natural forest fragments, compared to more intensively farmed, anthropogenic sites. In comparison, we observed eight lemur species in natural forest fragment sites in close proximity to the vanilla plantation sites, four of which we did not observe in any of the plantation sites. Our results provide evidence of lemurs using vanilla plantations and show that vanilla plantations may act as extensions of suitable habitat for lemurs, suggesting that they may also function as matrices between isolated forest fragments through which gene flow can occur. These are important and encouraging findings for both lemur conservation and for sustainable agroforestry undertaken by local farming communities.     

A possible role of plantations for primate conservation in Madagascar

The utilization of eucalyptus plantations by seven sympatric species of prosimians was studied in the eastern rainforest of Madagascar. The species were Avahi laniger, Cheirogaleus major, Hapalemur griseus, Indri indri, Lemur fulvus, Lepilemur mustelinus, and Microcebus rufus. None of the lemurs was ever found in young eucalyptus plantations with little undergrowth. This was mainly due to the lack of travel opportunities within the shrub layer and between the shrubs and the canopy. Food (mainly berries) is seasonally available in the shrub layer but cannot be exploited because frugivorous lemurs cannot reach it. Old eucalyptus plantations with dense undergrowth are used by all prosimian species. They provide food as well as travel and resting facilities. Mixed tree plantations in the western part of Madagascar were used by groups of Lemur fulvus, Lepilemur mustelinus, and Propithecus verreauxi. According to these results, old eucalyptus plantations and mixed tree species plantations could be used to provide firewood and construction wood for the human population. They also might extend the habitat for lemurs and serve as buffers against human disturbance.