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.     

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.     

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.     

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.     

Does Eulemur cinereiceps exist? Preliminary evidence from genetics and ground surveys in southeastern Madagascar

Although appearing in the literature as early as 1890, the brown lemur form Eulemur cinereiceps has recently resurfaced as a potentially valid taxon, distinct from neighboring, presumably closely related species such as white-collared lemurs (Eulemur albocollaris). We propose two scenarios for the potential separation of E. cinereiceps and E. albocollaris: (1) coastal and interior populations represent two distinct taxa and (2) the coastal population north of the Manampatrana River (the locality for purported museum specimens of E. cinereiceps) represents a distinct species from E. albocollaris found south of the river and in the interior escarpment forests. We tested these hypotheses using data from ground surveys and genetic sampling. Surveys were conducted in coastal forest fragments both north and south of the Manampatrana River in July-August 2006. Genetic samples were collected at two coastal sites and one interior forest. We used maximum parsimony, maximum likelihood, and neighbor-joining analyses on mitochondrial DNA regions to determine if populations from different sites clustered into diagnosable clades. Results from field surveys confirmed the presence of forms commonly referred to as E. albocollaris at the two southern coastal forests; no consistent phenotypic differences across sites were observed. All genetic analyses yielded identical results: coastal and interior populations do not cluster into separate groups, thus rejecting the first hypothesis. Eulemur species and all other day-active lemurs have apparently been extirpated from coastal forests north of the Manampatrana. Owing to the absence of lemurs from the northern coastal localities, we could not conclusively support or reject the second scenario. However, based on examination of the original plates and museum specimens, as well as the biogeographic patterns typical of this region, we strongly suspect that all populations from this area belong to a single species. We conclude with remarks regarding the apparent priority of E. cinereiceps for this taxon.     

Chromosomal evolution in Malagasy lemurs. IX. Chromosomal banding studies of Lepilemur mustelinus, L. dorsalis, and L. edwardsi

The karyotypes of three Lepilemuridae species, Lepilemur mustelinus, L. edwardsi, and L. dorsalis, are described and compared to those of three Lepilemur species previously reported. The phylogenetic relationships between the six species and their presumed last common ancestor are given. The results obtained, and the comparison with other groups, strongly suggest a monophyletic origin for all Malagasy lemurs.     

Isolation of sixteen autosomal loci and a sex-linked polymorphic microsatellite locus from the Milne-Edwards' sportive lemur (Lepilemur edwardsi)

We isolated 21 microsatellites from the Milne-Edwards' sportive lemur, Lepilemur edwardsi. Eighteen microsatellite sequences possessed sufficient flanking DNA for primer design. Seventeen loci amplified and were found to be polymorphic displaying two to 17 alleles in 32 unrelated individuals from a population from the National Park of Ankarafantsika in northwest Madagascar. One locus (Led-12) was found to be sex linked located on the X chromosome and can be used to sex-type 40% of female L. edwardsi lemurs. These 17 loci were characterized to investigate family structure and the phylogeography of L. edwardsi.     

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.     

Genetic Differentiation among Natural Populations of Lepilemur ruficaudatus

We studied the genetic differentiation of five populations of red-tailed sportive lemur Lepilemur ruficaudatus by means of allozyme variability and RAPD polymorphisms in order to test whether the Tsiribihina River separates the distribution areas of Lepilemur ruficaudatus and and L. edwardsi. Genetic data as well as the karyotype of a male individual clearly indicate that the Andramasay Forest in the north of Tsiribihina River is inhabited by Lepilemur ruficaudatus and not by L. edwardsi. We propose that the distribution of the two species are separated by the Manambolo River. However, the northernmost population of Lepilemur ruficaudatus inhabiting the Andramasay Forest is gentically differentiated from those that inhabit the dry forest in the south of Tsiribihina River.     

Defining the Low End of Primate Social Complexity: The Social Organization of the Nocturnal White-Footed Sportive Lemur (Lepilemur leucopus)

Whereas other species of sportive lemurs (genus Lepilemur) have been described as living in dispersed pairs, which are characterized by spatial overlap but a lack of affinity or affiliation between one adult male and female, existing reports on the social organization of the white-footed sportive lemur (Lepilemur leucopus) are conflicting, describing them as either living in dispersed one-male multifemale systems or pairs. We conducted this study in the spiny forest of Berenty Reserve, southern Madagascar, to clarify the social organization and to characterize the level of social complexity of this species. We combined 1530 h of radio-telemetry and behavioral observations over a period of 1 yr to describe the spatiotemporal stability, size, and interindividual overlap of individual home ranges as well as interindividual cohesiveness. Results revealed low intra- and high intersexual home range overlap. Although most of the social units identified consisted of dispersed pairs (N = 5), males were associated with two adult females in two cases. Furthermore, members of a social unit were never observed to groom each other or to share a daytime sleeping site, and Hutchinson’s and Doncaster’s dynamic interaction tests indicated active avoidance between pair partners. Low cohesiveness together with extremely low rates of social interactions therefore arguably places Lepilemur leucopus at the low end of primate social complexity.     

Resting metabolic rates of Lepilemur ruficaudatus

Seventeen sportive lemurs (Lepilemur ruficaudatus) were captured in a dry, deciduous forest in western Madagascar, and the resting metabolic rates were measured. According to the data, resting metabolic rates of Lepilemur ruficaudatus are among the lowest of mammalian folivores recorded so far. © 1996 Wiley-Liss, Inc.     

Crossing the uncrossable: novel trans‐valley biogeographic patterns revealed in the genetic history of low‐dispersal mygalomorph spiders (Antrodiaetidae,Antrodiaetus) from California

Antrodiaetus riversi is a dispersal‐limited, habitat‐specialized mygalomorph spider species endemic to mesic woodlands of northern and central California. Here, we build upon prior phylogeographic research using a much larger geographic sample and include additional nuclear genes, providing more detailed biogeographic insights throughout the range of this complex. Of particular interest is the uncovering of unexpected and replicated trans‐valley biogeographic patterns, where in two separate genetic clades western haplotypes in the California south Coast Ranges are phylogenetically closely related to eastern haplotypes from central and northern Sierran foothills. In both instances, these trans‐valley phylogenetic patterns are strongly supported by multiple genes. These western and eastern populations are currently separated by the Central Valley, a well‐recognized modern‐day and historical biogeographic barrier in California. For one clade, the directionality is clearly northeast to southwest, and all available evidence is consistent with a jump dispersal event estimated at 1.2–1.3 Ma. During this time period, paleogeographic data indicate that northern Sierran rivers emptied to the ocean in the south Coast Ranges, rather than at the San Francisco Bay. For the other trans‐valley clade genetic evidence is less conclusive regarding the mechanism and directionality of biogeographic exchange, although the estimated timeframe is similar (approximately 1.8 Ma). Despite the large number of biogeographic studies previously conducted in central California, to the best of our knowledge no prior studies have discussed or revealed a northern Sierran to south Coast Range biogeographic connection. This uniqueness may reflect the low‐dispersal biology of mygalomorph spiders, where ‘post‐event’ gene exchange rarely erases historical biogeographic signal.     

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.     

Phylogeography of the fiscal shrike (Lanius collaris): a novel pattern of genetic structure across the arid zones and savannas of Africa

Aim Savanna occupies a substantial part of Africa, being distributed around the two major tropical rain forest blocks in what is referred to as the Savanna Belt. Our current understanding of the genetic structure within species distributed across the Savanna Belt is primarily derived from mammalian taxa, studies of which have revealed a suture zone or transition between northern and east/southern Africa clades in south‐western Kenya and north‐western Tanzania. We conduct a phylogeographic study of the fiscal shrike (Lanius collaris), a polytypic species distributed across the Savanna Belt of Africa and for which morphological and vocal data are in agreement with the suture zone recovered for mammalian taxa, to test the hypothesis of a spatially congruent genetic break across several taxa, including birds. Location Africa, south of the Sahara. Methods We analysed DNA sequences recovered from four loci (one mitochondrial, two autosomal and one Z‐linked) in 66 individuals, representing all recognized subspecies, as well as putatively closely related species. We make use of a combination of tree‐building and population genetic methods to investigate the phylogeographic structure of the fiscal shrike across Africa. Results The fiscal shrike consists of two primary lineages with a strong geographic component: a northern group distributed from southern Tanzania to Senegal, and a southern group distributed from Botswana/Zambia to South Africa with isolated populations in Tanzania and northern Malawi. Unexpectedly, Souza’s shrike (L. souzae) was nested within L. collaris, as the sister group of the southern group. The positions of Mackinnon’s shrike (L. mackinnoni) and that of the São Tomé shrike (L. newtoni) were variable, being either nested within the fiscal shrike or sister to the L. collaris–L. souzae clade. Our divergence time analyses suggest that the Lanius collaris species complex started to diversify around 2.2 Ma. Main conclusions Our study reveals a distinct biogeographic pattern for a savanna distributed species in Africa, with the transition between the two primary genetic lineages occurring at a latitude of c. 15–16° S, 10° S further south than shown elsewhere for several mammalian species.     

Large scale patterns and trophic structure of southern African rocky shores: the roles of geographic variation and wave exposure

In this study we revise the biogeographic delimitation, and large-scale patterns of community structure of the intertidal rocky shores of southern Africa. We use binary (presence/absence) and per-species biomass data collected at fifteen localities and thirty-seven different rocky sites, encompassing the shores of southern Namibia, South Africa and southern Mozambique. Multivariate analyses revealed that the shores of southern Africa (south of 25°) can be divided into three main biogeographic provinces: the west coast or Namaqua province, the south coast or Agulhas province and the east coast or Natal province. The biomass structure of the intertidal rocky shores communities of southern Africa varied at a large scale, corresponding to biogeographic differences, while local-scale variation accorded with the intensity of local wave action. The average biomass of west coast communities was on average significantly greater than that of the south and east provinces. At a local scale, the community biomass on exposed shores was an order of magnitude greater than on sheltered shores, within all biogeographic provinces. Semi-exposed shores exhibited intermediate average biomass. The trophic structure of these communities varied significantly with wave action: autotrophs, filter-feeders and invertebrate predators were more prevalent on wave exposed than sheltered shores, whereas grazers were more abundant on sheltered and semi-exposed shores. Exposed shores were consistently dominated by far fewer species than semi-exposed and sheltered shores, independently of biogeographic differences. Within all biogeographic provinces semi-exposed and sheltered shores were more diverse than exposed shores. West coast intertidal communities therefore had high levels of biomass, but were consistently species-poor. Several working hypotheses that could explain these large and small-scale patterns are presented.     

Patterns of morphological and genetic variation in the endemic Malagasy bat Miniopterus gleni (Chiroptera: Miniopteridae), with the description of a new species, M. griffithsi

Over the past decade, major advances have been made concerning the systematics and species diversity of Malagasy bats, largely based on specimens collected during inventories and associated morphological and molecular genetic studies. Herein we describe a new species of endemic bat from southern Madagascar, Miniopterus griffithsi sp. n . , which is the sister taxa to Miniopterus gleni , a taxon described in 1995 (holotype from Sarodrano, just north of the Onilahy River in the southwest). Based on current information, M. griffithsi is found in the sub-arid bioclimatic zone, south of the Onilahy River, and M. gleni occurs in a variety of different bioclimatic zones, north of the Onilahy River to the northern portion of the island and on the near shore island of Ile Sainte Marie. The realization that M. griffithsi was a separate entity was first based on phylogeographic studies of the M. gleni complex. Comparisons using 397 bp of mitochondrial cytochrome b found a divergence of 1.2% within animals occurring across much of Madagascar north of the Onilahy River, 0.07% in those south of the Onilahy River, and 7.4% in populations separated by this river. Subsequently, morphological characters were identified that supported the specific separation of populations occurring south ( M. griffithsi ) and north of the Onilahy River ( M. gleni ), which include tragus shape, pelage coloration, and skull proportions.     

The Effects of Climate Seasonality on Behavior and Sleeping Site Choice in Sahamalaza Sportive Lemurs, <Emphasis Type="Italic">Lepilemur sahamalaza</Emphasis>

Temperature, rainfall, and resource availability may vary greatly within a single year in primate habitats. Many primate species show behavioral and physiological adaptations to this environmental seasonality, including changes to their diets and activity. Sahamalaza sportive lemurs (Lepilemur sahamalaza) inhabit the northwest of Madagascar and have been studied only during the dry, colder period of the year. We investigated potential effects of climate seasonality on this species by collecting behavioral data between October 2015 and August 2016, encompassing both the warmer wet and the colder dry seasons. We collected 773.15 hours of behavioral data on 14 individual sportive lemurs to investigate year-round activity budgets, ranging behavior, and sleeping site locations. Additionally we recorded temperature and rainfall data at our study site to describe the environmental conditions during the study period. The study individuals significantly decreased their time spent traveling and increased their time spent resting in the dry season compared to the wet season. Although home range size and path lengths did not differ over the study period, sleeping locations were significantly different between seasons as the lemurs focused on more confined areas in colder periods. Overall, the results indicate that Sahamalaza sportive lemur behavior varies with season, in line with reports for other primates.     

Second Sahelian amphibian endemism suggested by phylogeography of Groove crowned Bullfrog (Hoplobatrachus occipitalis) in western Sahel and hints of polyploid species formation

Several studies have assessed the phylogeographic patterns of vertebrates in North Africa and Sahara–Sahel, but most of the phylogeographic knowledge on amphibians comes from the Mediterranean region while the southern Sahara and Sahel remain poorly studied. Here, we assess the phylogeography of the African Groove crowned frog Hoplobatrachus occipitalis, with a focus on western Sahel in order to better understand the biogeographic patterns of semi-aquatic species in this arid region. Using mitochondrial and nuclear markers, we have assessed the species’ genetic structure, distribution of genetic diversity, and the presence of cryptic diversity. We found evidence of a recent (re-)colonization of the mountains in its northernmost distribution, but also for the role of southern Mauritanian mountains and large rivers as refugia. Two major lineages were detected, one perhaps endemic to Mauritania and the other widespread in Africa. The first lineage possibly constitutes the second Sahelian amphibian endemic; the latter may have originated through an allopolyploidy event, with the Mauritanian lineage being one of the parental ones.