Shawn M. Lehman

The Crisis of the Critically Endangered Greater Bamboo Lemur (Prolemur simus)

Abstract: Prolemur simus (the greater bamboo lemur) is the most abundant lemur in the northern subfossil sites of Madagascar. Living populations still persist, but in low numbers within a diminished range, making it one of the most critically endangered lemurs. Over the past twenty years scientists have searched the south- and central-eastern rain forests of Madagascar. Despite surveys that encompass over 500 km2, less than 75 animals have been found, with a recent total count of 60. More encouraging is that in 2007 two new sites containing P. simus were found: Mahasoa an unprotected 150 ha fragment east of the Ranomafana/Andringitra corridor (17 P. simus), and Torotorofotsy, a RAMSAR site near Andasibe (∼16 P. simus). Prolemur simus is a bamboo specialist with a patchy geographic distribution, which may be driven by the distribution of one or two bamboo species. Home ranges are large, group size has been observed to be from four to 26 individuals, and localities may be spaced hundreds of kilometers apart. Ranomafana National Park contains the only fully habituated group, and there are a total of three groups known in the park. We make recommendations for conservation action for these populations of P. simus. If immediate action is taken, we may be able to prevent the extinction of this species within the next decades.

Distribution and Diversity of Primates in Guyana: Species-Area Relationships and Riverine Barriers

Species-area relationships predict that there is a positive relationship between the number of species and the size of an area. It has been suggested that species richness will covary with area because larger areas have a greater diversity of habitats. Moreover, habitat diversity may operate in conjunction with riverine barriers to influence primate biogeography. Few studies have determined if and how these hypotheses relate to primate diversity in Guyana. To test these biogeographic hypotheses, I used data from 1,725 km of primate surveys I conducted in Guyana. I estimated geographic ranges for each of the 8 primate species via a GIS system. Geographic range size is a major determinant of the number of sightings of the 8 primate species. Primate species diversity is strongly negatively correlated with the number of rivers crossed moving in a clockwise pattern from eastern to NW Guyana. Interfluvial and habitat areas influence primate species diversity in Guyana. However, my data on primate biogeography in Guyana do not support the hypothesis that habitat diversity within the interfluvial areas effects primate diversity. Although the species-area relationship is considered the closest thing to a rule in ecology, researchers should be wary of too readily applying and accepting the model at all scales in biogeographic studies.

Primate Community Structure in Guyana: A Biogeographic Analysis

Studies of primate community structure increase our understanding of behavior, adaptation, and evolution. However, there are few biogeographic data on specific composition and association patterns in primate communities. I conducted a biogeographic analysis of the community structure of primate species at 16 sites in Guyana. I used data from 1725 km of line-transect censuses to determine specific composition and association patterns of 220 primate groups . Of the 18 polyspecific groups, 94.1% (N = 16) included squirrel monkeys. There was an overall trend towards positive specific associations among Guyanese primates. The only species that exhibited a negative pattern of interspecific associations were brown and wedge-capped capuchins. The sighting rate for wedge-capped capuchins at sympatric sites was particularly depressed compared to that for brown capuchins. Low plant productivity in Guyanese forests may reduce the diversity of feeding niches and result in a low incidence of polyspecific associations and scramble competition between wedge-capped and brown capuchins.

Colour and odour drive fruit selection and seed dispersal by mouse lemurs

Animals and fruiting plants are involved in a complex set of interactions, with animals relying on fruiting trees as food resources, and fruiting trees relying on animals for seed dispersal. This interdependence shapes fruit signals such as colour and odour, to increase fruit detectability, and animal sensory systems, such as colour vision and olfaction to facilitate food identification and selection. Despite the ecological and evolutionary importance of plant-animal interactions for shaping animal sensory adaptations and plant characteristics, the details of the relationship are poorly understood. Here we examine the role of fruit chromaticity, luminance and odour on seed dispersal by mouse lemurs. We show that both fruit colour and odour significantly predict fruit consumption and seed dispersal by Microcebus ravelobensis and M. murinus. Our study is the first to quantify and examine the role of bimodal fruit signals on seed dispersal in light of the sensory abilities of the disperser.

Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data

We tested four major hypotheses on the ecological aspects of body mass variation in extant Malagasy strepsirrhines: thermoregulation, resource seasonality/scarcity, resource quality, and primary productivity. These biogeographic hypotheses focus on the ecological aspects of body mass variation, largely ignoring the role of phylogeny for explaining body mass variation within lineages. We tested the independent effects of climate and resource-related variables on variation in body mass among Malagasy primates using recently developed comparative methods that account for phylogenetic history and spatial autocorrelation. We extracted data on lemur body mass and climate variables for a total of 43 species from 39 sites. Climatic data were obtained from the WorldClim database, which is based on climate data from weather stations compiled around the world. Using generalized linear models that incorporate parameters to account for phylogenetic and spatial autocorrelation, we found that diet and climate variables were weak predictors of lemur body mass. Moreover, there was a strong phylogenetic effect relative to the effects of space on lemur body mass in all models. Thus, we failed to find support for any of the four hypotheses on patterns of geography and body mass in extant strepsirrhines. Our results indicate that body mass has been conserved since early in the evolutionary history of each genus, while species diversified into different environmental niches. Our findings are in contrast to some previous studies that have suggested resource and climate related effects on body mass, though these studies have examined this question at different taxonomic and/or geographic scales.

Biogeography and Primates: A Review

In this paper, we present an introduction to primate biogeography at a continental level and then review the literature as it pertains to primate studies. Primate species diversity is highest in the Neotropics and Asia. Most primates range into rain/humid forests in Africa, Asia, and the Neotropics. Asia contains the highest total number of primate species (N = 38) that are considered to require conservation attention, followed closely by the Neotropics (N = 33 species). These biogeographic patterns reflect complex phylogenetic, geologic, and ecological processes. The various biogeographic theories and models used to explain these patterns can be organized into several broad categories (1) descriptive studies, (2) comparative-quantitative approaches, (3) refugia theory, (4) phylogenetic approaches, (5) community ecology, and (6) conservation biology. Descriptive models have been derived from distribution data obtained during collecting expeditions. These models focused on geographic variations in species characteristics and barriers to dispersal (e.g., Gloger’s Rule, Bergmann’s Rule, Allen’s Rule, river barrier hypothesis). With the advent of digitized statistical procedures, these barriers became testable biogeographic hypotheses using comparative-quantitative models. Thus, many researchers have noted the importance of rivers as geographical subdivisions of populations of a species. Comparative-quantitative models have also involved studies of species-area and distribution-abundance relationships. Generally, larger areas are more species rich and widely distributed primates tend to exist at higher densities. Many researchers have also investigated various ecological correlates (e.g., rainfall, latitude) to patterns of primate species richness. There has been considerable debate regarding the importance of Pleistocene Refugia for understanding the historical biogeography of primates. Phylogenetic or cladistic biogeography focuses on shared derived characters, which can be used to reconstruct biogeographical history. The presence or absence of species within a geographic area has been investigated extensively through studies of community ecology. Similarities between primate communities are most likely if they share a common biogeographic history. Composition of primate communities can also reflect evolutionary niche dynamics. Finally, researchers studying primate conservation biology have synthesized methods from various biogeographic models to understand and predict primate rarity and extinction events. Much of the renewed interest in primate biogeography tends to focus on the spatial and temporal patterns that influence species origins and diversity.

Feeding Patterns in a Small-Bodied Nocturnal Folivore (Avahi laniger) and the Influence of Leaf Chemistry: A Preliminary Study

We present data on feeding patterns in Avahi laniger and compare these data to temporal variations in leaf chemistry. Because A. laniger is one of the smallest folivorous primates and has a monogastric stomach, we hypothesized that this lemur would display behavioural adaptations to a leaf-based diet by scheduling feeding times when leaves were of highest quality. Data were collected from May to August 2004 at the Vatoharanana site in Ranomafana National Park, Madagascar. A. laniger fed during different time periods despite leaf carbohydrate and protein concentrations exhibiting little variation throughout the night. Although tannin concentrations exhibited temporal fluctuations, they did not covary with A. laniger feeding times. We suggest that A. laniger feeding times cannot be explained entirely by variations in leaf chemistry.

Biogeography of the Primates of Guyana: Effects of Habitat Use and Diet on Geographic Distribution

Species that exploit a wide range of resources or habitats (generalists) tend to be widely distributed, whereas species that exploit a narrow range of resources or habitats (specialists) often have a limited distribution. The distribution patterns are thought to result from specialists using relatively smaller habitats than those exploited by generalists. I used data from 1,725 km of primate surveys that I conducted in Guyana to test these hypotheses. Habitat breadth is the total number of different habitat types occupied by each species. I used the total number of different food categories exploited by each species to measure dietary breadth. Geographic range size is correlated with habitat breadth but not with dietary breadth or body size for the 8 primate species in Guyana. Habitat generalists—red howlers and wedge-capped capuchins—range into all habitats. Habitat specialists—spider monkeys, brown bearded sakis, and golden-handed tamarins—range only into large habitats. Habitat generalists tend to be dietary type specialists in Guyana. I suggest that only habitat generalists can subsist on the low-quality foods in small habitats in Guyana. Conversely, habitat specialists tend to be dietary type generalists in Guyana. They must feed on a variety of food types in large habitats. However, using the number of food categories exploited as a measure of dietary breadth may be only a weak aspect of multidimensional niche. Researchers testing biogeographic hypotheses associated with dietary breadth should consider including multivariate indicators of both the types of food categories eaten and the number of plant species exploited.

Spatial Variations in Eulemur fulvus rufus and Lepilemur mustelinus Densities in Madagascar

I present data on variations in Eulemur fulvus rufus and Lepilemur mustelinus densities as well as tree characteristics (height, diameter and stem frequency) between edge and interior forest habitats in southeastern Madagascar. Line transect surveys were conducted from June 2003 to November 2005 in edge and interior forest habitats in the Vohibola III Classified Forest. Although E. f. rufus densities were significantly lower in edge habitats than in interior habitats, density estimates for L. mustelinus did not differ significantly between habitats. Trees in edge habitats were significantly shorter, had smaller diameters and had lower stem frequencies (for those >25 cm in diameter) than trees in interior habitats. Spatial characteristics of food abundance and quality may explain lemur density patterns in Vohibola III. Low E. f. rufus densities may reduce seed dispersal in edge habitats, which has important consequences for the long-term viability of forest ecosystems in Madagascar.

Edge Effects on Foliar Stable Isotope Values in a Madagascan Tropical Dry Forest

Edge effects represent an inevitable and important consequence of habitat loss and fragmentation. These effects include changes in microclimate, solar radiation, or temperature. Such abiotic effects can, in turn, impact biotic factors. They can have a substantial impact on species, communities, and ecosystems. Here we examine clinal variations in stable carbon and nitrogen isotope values for trees along an edge-interior gradient in the dry deciduous forest at Ankarafantsika National Park. We predicted that soil respiration and differences in solar irradiance would result in stratified δ13C values where leaves collected close to the forest floor would have lower δ13C values than those growing higher up in the canopy. We also anticipated that plants growing at the savannah-forest boundary would have higher δ13C and δ15N values than plants growing in the forest interior. As expected, we detected a small but significant canopy effect. Leaves growing below 2 m from the forest floor exhibit δ13C values that are, on average, 1.1‰ lower than those growing above this threshold. We did not, however, find any relationship between foliar δ13C and distance from the edge. Unpredictably, we detected a striking positive relationship between foliar δ15N values and increasing distance into the forest interior. Variability in physiology among species, anthropogenic influence, organic input, and rooting depth cannot adequately explain this trend. Instead, this unexpected relationship most likely reflects decreasing nutrient or water availability, or a shift in N-sources with increasing distance from the savannah. Unlike most forest communities, the trees at Ampijoroa are growing in nutrient-limited sands. In addition to being nutrient poor, these well-drained soils likely decrease the amount of soil water available to forest vegetation. Continued research on plant responses to edge effects will improve our understanding of the conservation biology of forest ecosystems in Madagascar.