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.     

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.     

Molecular Evidence of Reproductive Isolation in Sympatric Sibling Species of Mouse Lemurs

Recent morphological and molecular phylogenetic studies of mouse lemurs (Microcebus) living in the western and southern regions of Madagascar have shown that specific diversity had been considerably underestimated. In large part, this underestimate was due to the lack of sufficient specimens from given localities to assess properly the level of phenotypic variation within and between populations. The accurate delineation of specific boundaries has no doubt been confounded by the diminutive size, nocturnal habits, and subtle morphological variation characteristic of mouse lemurs, which can make field identification of individuals problematic. We illustrate the use of molecular phylogenetic analysis to reveal reproductive isolation in two sympatric mouse lemur species, Microcebus murinus and M. griseorufus. Their documentation in the Berenty Private Reserve in the extreme south of Madagascar verifies the historically-broad distribution of Microcebus griseorufus, a species recently resurrected from synonomy.     

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.     

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.     

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 role of zoos and captive breeding in lemur conservation

All the lemurs of Madagascar are declining in the wild, but the species and numbers held in collections outside Madagascar are not sufficient to ensure the continuence of their genetic diversity in captivity. General recommendations as to how to rectify this situation are presented, including a strong plea for coordinated population management among collections holding lemurs.     

Unexpected species diversity of Malagasy primates (<Emphasis Type="Italic">Lepilemur</Emphasis> spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species

Background  

The lemurs of Madagascar provide an excellent mammalian radiation to explore mechanisms and processes favouring species diversity and evolution. Species diversity, in particular of nocturnal species, increased considerably during the last decade. However, the factors contributing to this high diversity are not well understood. We tested predictions derived from two existing biogeographic models by exploring the genetic and morphological divergence among populations of a widely distributed lemur genus, the sportive lemur (Lepilemur ssp.) along a 560 km long transect from western to northern Madagascar.     

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.     

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.     

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.     

The secrets of lemur teeth

New tools are available for teasing out aspects of life‐history variation among extinct species. Here we summarize research on the life histories of the extinct lemurs of Madagascar. There is a wide range of variation in dental developmental timing among these species, from among the most accelerated (Palaeopropithecus) to among the most prolonged (Hadropithecus) within the Order Primates. Rather than reflecting variation in body size, this diversity appears to relate to niche characteristics and encephalization.     

Morphological Variation in Populations of <Emphasis Type="Italic">Eulemur albocollaris</Emphasis> and <Emphasis Type="Italic">E. fulvus rufus</Emphasis>

Sexual dimorphism in body size and canine weaponry is commonly associated with high levels of male-male competition. When group living species do not rely heavily on male-male competition for access to females, sperm competition may represent a viable alternative strategy. Unlike most haplorhine primates, lemurs are typically monomorphic in body weight and canine height. We assessed variability of body mass dimorphism and canine size dimorphism in brown lemurs using morphometric data from 3 populations in southeastern Madagascar: Eulemur fulvus rufus, E. albocollaris, and hybrids of the species. We found significant male-biased canine dimorphism in E. albocollaris in conjunction with body-size monomorphism. We observed similar patterns in the hybrids, but E. fulvus rufus exhibited significant female-biased size dimorphism and canine monomorphism. Testes volume was relatively high across study populations. Thus, sperm competition appears to be strong in brown lemurs. E. albocollaris males combine sperm competition with large canines, but not higher body mass, indicating a difference in sexual strategy from most lemurs. Patterns of body mass and canine size dimorphism are not uniform across brown lemur populations, indicating that future work on these populations can explicitly test models that predict relationships between size dimorphism and various types of competition.     

Some observations of two kinds of lemuridae (Varecia variegata variegata andLemur fulvus albifrons) in the reserve of Nosy Mangabe

A total of nine groups of ruffed lemurs (Varecia variegata variegata), as well as one solitary individual, were observed on Nosy Mangabe, an island located off the eastern coast of Madagascar, for a total 536 min between November 30 and December 8, 1983. The average group size was 2.8 animals (N=5), and the population density was 175 animals/km², as estimated from direct observation and location of vocalization. During the same period, nine groups of brown lemurs (Lemur fulvus albifrons) and one solitary individual were observed for a total 320 min. One group of brown lemurs was composed of eight animals (two adult males and females, one male juvenile, two infants, and one individual of undetermined age and sex). Feeding competition occurred between the two species, with whichVarecia variegata variegata dominating.     

The first report of <Emphasis Type="Italic">Spondias</Emphasis> native to Madagascar: <Emphasis Type="Italic">Spondias tefyi</Emphasis>, sp. nov. (Anacardiaceae)

Spondias represents a genus new to Madagascar’s native flora. Like Campnosperma, it is now known from both American and Asian tropics and Madagascar but not from continental Africa. The new species Spondias tefyi is easily distinguished from all of its Asian congeners by having the stamens shorter than the pistil and fruits brown and lenticellate at maturity (vs. greenish, yellow, orange or red, and relatively smooth). The new species is one of several Anacardiaceae whose fruits are eaten by lemurs in the Analavelona Forest, highlighting the importance of conserving this threatened subhumid forest remnant in southern Madagascar.     

Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur ( Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur ( Microcebus rufus) in Eastern Madagascar

To investigate for the first time the relationship between contrasting patterns of seasonal changes of the environment and activity, body mass and reproduction for small nocturnal primates in nature, we compared a population of golden brown mouse lemur (Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar and of the brown mouse lemur (Microcebus rufus) in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions. Golden brown mouse lemurs (GBML) were active during the whole period (May to December) irrespective of changing environmental conditions. In contrast, a part of the population of brown mouse lemurs (BML) showed prolonged seasonal torpor, related to body mass during periods of short day length and low ambient temperatures. Differences between species might be due to differences in ambient temperature and food supply. Body weight and tail thickness (adipose tissue reserve) did not show prominent differences between short and long photoperiods in GBML, whereas both differ significantly in BML, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species showed a seasonal reproduction. The rate of growth and size of the testes were similar and preceded estrous onset in both species suggesting a photoperiodic control of reproduction in males. The estrous onset in females occurred earlier in GBML than in BML. Estrous females were observed over at least 4 months in the former, but in only 1 month in the latter species. Intraspecific variation of estrous onset in GBML may be explained by body mass. Interspecific variation of female reproduction indicates species-specific differences in the control of reproduction. Thus, environmentally related differences in annual rhythms between closely related small nocturnal lemurs emerged that allow them to cope with contrasting patterns of seasonal changes in their habitats.     

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.     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Antipredator behavior in lemurs: Evidence of an extinct eagle on Madagascar or something else?

Goodman (1994) related the antipredator response exhibited by two species of lemurs from southwestern Madagascar against extant birds of prey to the predatory efforts of an extinct eagle, inhabiting the same region about 4000 years ago. He argued that today’s smaller raptors, hunting young individuals perhaps only occasionally, represent marginal danger to lemurs. Nevertheless,their activity would be sufficient to impose a continuous reinforcement to a strong antipredator response. I question such an interpretation and instead suggest that extant birds of prey may indeed represent a strong threat to lemurs and that the same might not have been necessarily true for the extinct eagle. In addition, I propose four optional hypotheses, all of which encompass a marginal role for the extinct eagle.