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.     

Elevational Ranges of Lemurs in the Humid Forests of Madagascar

The geological history of Madagascar contains events that may have given rise to unusual factors that molded the primate communities of the island. In order to understand the impact of the factors we reviewed the elevational distribution of extant primate species in the humid forests. The elevational structuring of primates in the humid forests of Madagascar shows considerable differences from other tropical areas in the New World and Asia, which is correlated with the lack of large tracts of humid lowland habitat on Madagascar since it split from India.     

Lemur Diversity in Madagascar

A basic understanding of the taxonomy, diversity, and distributions of primates is essential for their conservation. This review of the status of the taxonomy of lemurs is based on a 5-d workshop entitled “Primate Taxonomy for the New Millennium,” held at the Disney Institute, Orlando, Florida, in February 2000. The aim is not to present a taxonomic revision, but to review our current understanding of the diversity and current and past ranges of lemurs and indicate where there is controversy, discrepancy, or lack of knowledge. Our goal therefore is to provide a baseline for future taxonomic investigation, as well as a clearer focus for research and conservation priorities. We here focus on the lemurs of Madagascar and recognize 5 families, 15 genera, and 99 species and subspecies. We list 39 species of lemurs described since 2000: 2 dwarf lemurs, Cheirogaleus; 11 mouse lemurs, Microcebus; a giant mouse lemur, Mirza; a bamboo lemur, Hapalemur; 17 sportive lemurs, Lepilemur; and 7 woolly lemurs, Avahi. Taxonomic revisions have resulted in the resurrection of a further 9 taxa. However, the figures do not represent the total diversity of Malagasy lemurs because more new species are being identified via new field studies and accompanying genetic research, and should be described in the near future.     

Effects of Transect Selection and Seasonality on Lemur Density Estimates in Southeastern Madagascar

I investigated how transect type (trails vs. cut transects) and seasonality influenced density estimates for 5 lemur taxa (Avahi laniger, Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus) in the Vohibola III Classified Forest in SE Madagascar. I surveyed tree height and diameter and lemur populations from June 1 to December 28, 2004 along 2 1250-m trails local people used and 2 1250-m transects cut parallel to the trails in primary rain forest. Despite dendrometric variations within and between trails and transects, only density estimates of Hapalemur griseus griseus differed significantly by transect type. The spatial variation may be a result of removal by local people of giant bamboo, which is the main food for Hapalemur griseus griseus, along trails. Conversely, seasonality influenced density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus. The temporal variations may be related to seasonal torpor for Cheirogaleus major and increased detection probabilities during periods of fruit exploitation for Eulemur rubriventer, Microcebus rufus, and Hapalemur griseus griseus. Transect type and seasonality did not affect density estimates for Avahi laniger, which may be related to the highly folivorous and low-energy diet of the nocturnal lemur. Researchers surveying lemurs along line transects should be aware that transect selection may influence density estimates for Hapalemur griseus griseus and that seasonality may influence density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus.     

Relationship Between Microhabitat Structure and Distribution of Mouse Lemurs (Microcebus spp.) in Northwestern Madagascar

Understanding processes affecting the distribution and abundance of organisms is a central issue in ecology and conservation biology. In northwestern Madagascar, we found an uneven distribution pattern of the golden-brown mouse lemur (Microcebus ravelobensis) and the grey mouse lemur (M. murinus). In one area (JBA) the two species lived sympatrically, whereas in another forest area (JBB) Microcebus ravelobensis occurred exclusively. To investigate whether differences in forest structure may explain this uneven distribution, we conducted a microhabitat analysis and related it to specific distribution. In JBA the habitat of Microcebus ravelobensis was characterized by a higher percentage of trees with many lianas and a higher cover of the herb layer, whereas that of M. murinus had a higher number of trees with a diameter at breast height (DBH) >10 cm. The comparison of the forest structure of the microhabitats of the two species between JBA and JBB revealed further differences. The cover of the overstory, the percentage of trees without lianas and the number of larger trees (DBH >10 cm) among the microhabitats were higher for Microcebus murinus in JBA than for M. ravelobensis in JBB whereas the microhabitats of M. ravelobensis at the two sites did not differ concerning these vegetation structures. Differences between the two species coincide with those of resources important for survival. Our results indicate the importance of microhabitat analyses for the understanding of distribution patterns of species and for successful conservation planning.     

Habitat Characteristics and Lemur Species Richness in Madagascar1

In the extant lemur communities of Madagascar the number of lemur species increases with increasing number of tree species. In forests with few tree species lemurs use patches with higher number of tree species than average. However, in forest plots with high number of tree species, lemurs stay in places with lower number of tree species than average. At low tree species diversity a minimum number of different tree species seems to be required within the animals' home range to assure year-round food availability. At high tree species diversity tree species essential for survival might be diluted by resources which are of no use for lemurs, thus increasing energetic expenses for traveling between suitable patches. According to the present analyses, structural diversity is of subordinate importance to the number of tree species as a correlate of lemur species richness. Within limits of disturbance intensity and on a small geographic scale, disturbances increase forest productivity. Lemurs reach higher species numbers and population densities in slightly disturbed areas compared with undisturbed sites. This peaked curve of the number of lemur species over disturbance, however, may not only be a consequence of “resource dilution” in undisturbed sites and higher food abundance in slightly disturbed areas, but also a consequence of selective extinction of lemur species which were unable to cope with the disturbance regime exaggerated by human interference over the last few hundred or thousand years.     

Trends in forest fragment research in Madagascar: Documented responses by lemurs and other taxa

The rise in research investigating fragmentation and its impact on primates and other taxa reflects the growing presence of fragmented landscapes themselves. Although numerous studies report the negative effects of fragmentation on biodiversity, it is difficult to generalize responses to fragmentation for specific taxonomic groups, such as non-human primates, when studies have not employed a definitive concept of fragmentation or fragments themselves. Madagascar's high degree of fragmentation, wealth of endemic taxa, and extensive history of ecological research provide the opportunity to compare fragmentation studies across similar contexts. We conducted a literature search of peer-reviewed articles on fragmentation in Madagascar to characterize its trends. A total of 70 articles, 46 of which concentrated on lemurs, tested the impacts of fragmentation on Malagasy taxa, while additional sources conducted research in one or more fragments without testing its effects (n = 112 total, 79 on lemurs). Studies on lemurs most frequently tested fragmentation's impacts on genetics and biodiversity metrics (n = 16 and 15 studies, respectively), although health, modeling, behavioral, and cross-disciplinary techniques were also reported. Responses to fragmentation were reported for 49 lemur species, with most studies concentrated in eastern Madagascar (87%). Although there was variation in the metrics reported in studies testing the effects of fragmentation on Malagasy species, the most common measures were fragment area, isolation, or comparison to a control site. Landscape-scale approaches and examination of fragmentation per se were rarely employed. Characterizing trends of fragmentation research in Madagascar emphasizes the challenges of documenting fragmentation's effects while highlighting the benefits of research within fragmented landscapes, particularly when combined with consideration for how the matrix within human-modified landscapes may impact primate populations.     

The Obvious Aspects of Ecological Underprivilege in Ankarana, Northern Madagascar

On the basis of research conducted in the Ankarana region of northern Madagascar, I discuss the speculating that Malagasy participants in the local sapphire trade do about foreign ecotourists who come to this region. Although some have been promoting international ecotourism in the region as a viable means to a sustainable future for local people and ecosystems, others, including many of the observers discussed here, see the rise of the ecotourist trade and the increasing presence of its clients in Ankarana as signs of foreigners' long-standing interests in Malagasy resources. I argue that to understand the perspectives of these critical observers, it is necessary to appreciate what they take to be obvious about ecotourism and the conservation projects with which they are commonly associated.     

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.     

Realized distribution patterns of crowned lemurs (Eulemur coronatus) within a human-dominated forest fragment in northern Madagascar

Due to the impact of anthropogenic activities on forest extent and integrity across Madagascar, it is increasingly necessary to assess how endangered lemur populations inhabiting human-dominated forest fragments can effectively sustain themselves ecologically. Our research addresses this concern by exploring how the distribution patterns of a small population of crowned lemurs (Eulemur coronatus), occupying a degraded forest fragment at Oronjia Forest New Protected Area in northern Madagascar, are impacted by the availability of key ecological and anthropogenic factors. We hypothesize that the distribution of E. coronatus within the fragment is limited by the availability of critical ecological resources and conditions and the intensity of anthropogenic features and activities. To examine this, we used MaxEnt to develop a species distribution model using presence-only occurrence records and 10 independent background covariates detailing the site's ecological and anthropogenic aspects. The results indicate that the realized distribution patterns of E. coronatus within human-dominated forest fragments are strongly associated with sections of forest that contain sparsely and sporadically distributed resources, such as freshwater and continuous hardwood vegetation. We conclude that the distribution of E. coronatus at Oronjia is shaped by their need to maximize foraging opportunities in a degraded forest landscape where they are subject to both environmental and anthropogenic stressors.     

Taxonomic Revision of Mouse Lemurs (Microcebus) in the Western Portions of Madagascar

The genus Microcebus (mouse lemurs) are the smallest extant primates. Until recently, they were considered to comprise two different species: Microcebus murinus, confined largely to dry forests on the western portion of Madagascar, and M. rufus, occurring in humid forest formations of eastern Madagascar. Specimens and recent field observations document rufous individuals in the west. However, the current taxonomy is entangled due to a lack of comparative material to quantify intrapopulation and intraspecific morphological variation. On the basis of recently collected specimens of Microcebus from 12 localities in portions of western Madagascar, from Ankarana in the north to Beza Mahafaly in the south, we present a revision using external, cranial, and dental characters. We recognize seven species of Microcebus from western Madagascar. We name and describe 3 spp., resurrect a previously synonymized species, and amend diagnoses for Microcebus murinus (J. F. Miller, 1777), M. myoxinus Peters, 1852, and M. ravelobensis Zimmermann et al., 1998.     

Population and social dynamics changes in ring-tailed lemur troops at Berenty,Madagascar between 1989 - 1999

In the present study, we recorded all births, immigrations, deaths, and emigrations for a population of ring-tailed lemurs at Berenty Reserve, Madagascar, between September 1989 and August 1999. In September 1989, three troops (C, B, and T) inhabited the study area of 14.2 ha. During the 10-year period, eight troop divisions, six evictions of females, and three troop takeovers of ranges by other troops occurred in and around the study area. Consequently, in August 1999, the number of troops in the same area increased to six (CX, C1, C2A, C2B, T1, and T2). The number of lemurs aged >1 year increased from 63 to 82, which resulted from 204 births, 58 immigrations, 125 deaths, and 118 emigrations. Of the 204 newborn lemurs during the study period, 103 died, 44 emigrated outside the study area, and 57 remained within the study area. The total number of lemurs that emigrated from natal troops was 69 (54 males and 15 females). Natal males left their troops around the age of 3. Non-natal males changed troops after a tenure varying from 1 to 7 years. Survival curves showed a fall in survival rates of both sexes to < 0.5 between the ages of 2 and 3. For females, the survival rate gradually decreased to < 0.2 at the age of 9. On the other hand, due to emigration, the survival rate of males could not be determined after the age of 5 yr. Since some males attained high-rank at the age of 6 – 10 yr, the prime age for male ring-tailed lemurs is thought to be around 7 – 10 yr. Ring-tailed lemurs are essentially female philopatric, because all cases of females leaving natal troops resulted from troop divisions or forced evictions. Such social changes may have resulted from competition among females. All cases of troop divisions or evictions occurred in larger troops consisting of ≥20 lemurs, and only a few females could rejoin their troops. When males joined such a female-group, a new troop was formed. Although promoted by an increase in population, frequent emigrations of females from original troops are the characteristics of ring-tailed lemurs at Berenty.     

Biogeography of Dwarf Lemurs: Genetic Evidence for Unexpected Patterns in Southeastern Madagascar

Seven species of dwarf lemurs (Cheirogaleus spp.) are currently recognized after a recent revision of the genus. During a field study in southeastern Madagascar, we observed 3 distinct morphotypes of Cheirogaleus resembling Cheirogaleus medius, C. major and C. crossleyi. In particular, for Cheirogaleus crossleyi southeastern Madagascar was far away from the known distribution range of the species when referring to the recent revision of the genus. In order to clarify the taxonomic status of the 3 morphotypes, we compared field samples from southeastern Madagascar to museum specimens from several locations in Madagascar and to field samples from Kirindy/CFPF, western Madagascar by genetic analyses using the mitochondrial cytochrome b gene. Genetic data yield strong support for 2 of the 3 morphotypes to represent Cheirogaleus medius and C. major. The third morphotype is genetically closely related to Cheirogaleus crossleyi, albeit more distantly than the other 2 morphotypes to the respective reference samples. The genetic distance is related to a considerable geographic distance between the location of our field study and the origin of the respective reference specimen, because Cheirogaleus crossleyi had been reported only from northern Madagascar. Our field observations indicate an isolated population in southeastern Madagascar. We propose to identify them as Cheirogaleus crossleyi and discuss the population genetic and biogeographic considerations supporting this conclusion.     

Ecological Correlates to Lemur Community Structure in Southeast Madagascar

The Fandriana-Marolambo forest corridor is one of the largest (ca. 250,000 ha) and least explored tracts of unprotected forest in southeast Madagascar. Although published range maps show continuous distributions for many lemurs throughout the region, there are few data on lemur community structure in the corridor. We aimed to determine lemur community structure, with its ecological correlates (altitude, agriculture, selective logging, and hunting), in the Fandriana-Marolambo forest corridor. We surveyed 7 sites and sighted 4 nocturnal taxa (Avahi laniger, Cheirogaleus major, Lepilemur mustelinus, and Microcebus rufus) and 6 diurnal taxa (Eulemur rubriventer, E. fulvus rufus, E. f. fulvus, Propithecus diadema edwardsi, Hapalemur griseus griseus, and Varecia variegata variegata). Composition of the lemur community was broadly similar to that of nearby protected areas (Ranomafana and Mantadia National Parks). However, we sighted no Hapalemur aureus, H. simus, or Indri indri, and observed Propithecus diadema edwardsi and Varecia variegata variegata at only 1 site each. We sighted an apparent hybrid form of Eulemur fulvus fulvus and E. f. rufus that may represent a new hybrid zone for lemurs. After testing for spatial autocorrelation, lemur diversity correlates negatively with altitude and agricultural intensity. Though the Government of Madagascar is assessing the corridor as a new national park, we suggest conservation plans for local lemurs are complicated by population isolation and lack of data on minimum viable size of the proposed protected area.     

Predation as a landscape effect: the trading off by prey species between predation risks and protection benefits

1. Predators impose costs on their prey but may also provide benefits such as protection against other (e.g. nest) predators. The optimal breeding location in relation to the distance from a nesting raptor varies so as to minimize the sum of costs of adult and nest predation. We provide a conceptual model to account for variation in the relative predation risks and derive qualitative predictions for how different prey species should respond to the distance from goshawk Accipiter gentilis nests. 2. We test the model predictions using a comprehensive collection of data from northern Finland and central Norway. First, we carried out a series of experiments with artificial bird nests to test if goshawks may provide protection against nest predation. Second, we conducted standard bird censuses and nest-box experiments to detect how the density or territory occupancy of several prey species varies with distance from the nearest goshawk nest. 3. Nest predation rate increased with distance from goshawk nest indicating that goshawks may provide protection for birds' nests against nest predation. Abundance (or probability of presence) of the main prey species of goshawks peaked at intermediate distances from goshawk nests, reflecting the trade-off. The abundance of small songbird species decreased with distance from goshawk nests. The goshawk poses little risk to small songbirds and they may benefit from goshawk proximity in protection against nest predation. Finally, no pattern with distance in pied flycatcher territory (nest box) occupation rate or the onset of egg-laying was detected. This is expected, as flycatchers neither suffer from marked nest predation risk nor are favoured goshawk prey. 4. Our results suggest that territory location in relation to the nest of a predator is a trade-off situation where adult birds weigh the risk of themselves being predated against the benefits accrued from increased nest survival. Prey species appear able to detect and measure alternative predation risks, and respond adaptively. From the prey perspective, the landscape is a mosaic of habitat patches the quality of which varies according to structural and floristic features, but also to the spatial distribution of predators.     

Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar

I aimed to determine when and under which seasonal environmental conditions gray mouse lemurs (Microcebus murinus), a small nocturnal primate species endemic to Madagascar, utilize daily torpor. Using temperature-sensitive radio collars, I measured skin temperature (T _sk ) of free-ranging mouse lemurs under natural conditions. My results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a ) during the dry season, but not during the rainy season. Mouse lemurs that remained normothermic had significantly lower body masses (mean: 59.7 g) than individuals that used torpor (mean: 80.2 g). Skin temperatures dropped to 20.9°C and the mean torpor bout duration is 10.3 h. The use of torpor on a given night varied among individuals, whereas the propensity for torpor did not differ significantly between males and females. I found no evidence that T _a can be used to predict whether mouse lemurs will remain normothermic or enter torpor. It appears that the most reliable indicator for the occurrence of torpor in free-ranging Microcebus murinus is time of the year, i.e., photoperiod.     

Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

Phenology of the Littoral Forest of Sainte Luce,Southeastern Madagascar1

From January 2000 through December 2002, focal plant censuses were carried out to assess monthly leaf, flower, and ripe fruit presence for 423 individual plants (96 plant species, 39 families) within the littoral forest of Sainte Luce, Madagascar. Fruit‐on‐trail counts were conducted additionally in 2000 to allow comparison between both phenological methods. Despite low climatic seasonality and the absence of a dry season in the littoral forest, interannual phenological patterns were seasonal. Within year variability was present with clear periods of abundance and scarcity. All phenophases were highly intercorrelated and peaked from November through February. This was found in other humid Malagasy forests as well, while in dry Malagasy forests phenophases were separated in time perhaps due to the more seasonal climate. Temperature and day length seemed to influence all phenophases, the latter showing the strongest effect, while rainfall was only weekly associated with flushing and flowering. Differences in the presence of ripe fruits when comparing between sampling methods can be explained by the differential contribution of several life forms.