Steig E. Johnson

The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS

204 Abstract The unique primates of south-eastern Madagascar face threats from growing human popula- tions. The countrys extant primates already represent only a subset of the taxonomic and ecological diversity existing a few thousand years ago. To prevent further losses remaining taxa must be subjected to effective monitoring programmes that directly inform conserva- tion efforts. We offer a necessary first step: revision of geographic ranges and quantification of habitat area and population size for diurnal and cathemeral (active during both day and night) lemurs. Recent satellite images are used to develop a forest cover geographical information system, and censuses are used to establish range boundaries and develop estimates of population density and size. These assessments are used to identify regions and taxa at risk, and will be a useful baseline for future monitoring of habitat and populations. Precise estimates are impossible for patchily-distributed taxa (especially Hapalemur aureus, H. simus and Varecia variegata variegata); these taxa require more sophisticated modelling.

Positional behavior and vertebral morphology in atelines and cebines

Atelines are of particular interest to primate evolutionary studies because they converge with hominoids in postcranial anatomy, including the vertebral column. Currently, our understanding of ateline vertebral morphology is limited to mainly qualitative descriptions and functional interpretations based on general categories of positional behavior. Even less is known about the vertebrae of other platyrrhines. This study more closely examines vertebral form and function in atelines and cebines by combining direct field observations of axial postures and movements, assessments of spinal loading regimes, and a detailed vertebral morphometric analysis. Field observations (Corcovado, Costa Rica) on Ateles geoffroyi, Alouatta palliata, Cebus capucinus, and Saimiri oerstedii were quantified in conjunction with a morphometric analysis of ateline and cebine lumbar vertebrae. Hylobates was also included for comparison. Compared to Cebus and Saimiri, atelines engage more frequently in postures and locomotor behaviors that induce pronounced bending loads on the spine. All atelines share lumbar adaptations for resisting bending, including ventrodorsally elongated vertebral bodies and perpendicularly oriented transverse processes. Among atelines, lumbar region lengths and vertebral bodies are shortest in Ateles and Brachyteles, longest in Alouatta (resembling Cebus), and intermediate in Lagothrix. Compared to Cebus and all atelines, Saimiri has a relatively longer lumbar region, longer and less ventrodorsally expanded vertebral bodies, and more ventrally oriented transverse processes. These features accentuate bending loads, but increase the sagittal flexibility required for leaping. Vertebral convergence between hylobatids and atelines is more readily interpretable as a product of shared spinal loading patterns than shared positional behaviors.

Census of brown lemurs (Eulemur fulvus sspp.) in southeastern Madagascar: Methods-testing and conservation implications

Four forest areas were censused in southeastern Madagascar from June–August 1995 to estimate local population densities and habitat conditions for two threatened subspecies of brown lemur (Eulemur fulvus collaris and Eulemur fulvus albocollaris). Survey transects varied in length (1–3.5 km) and in surveillance frequency (three to seven times). Additional test surveys were conducted at the Parc National de Ranomafana to compare transect methods in an area with known population densities of Eulemur fulvus. Based on these tests, we demonstrate that the use of existing trails for transects can result in a close estimate of local population size, although more replications and longer transects increase precision. Results from regional surveys indicate considerably smaller population densities for E. f. albocollaris (0.086 animals/ha). In contrast, E. f. collaris densities were relatively high (.107 animals/ha) at Midongy‐Sud. We also noted variation among sites in the density of lianas, which was positively correlated with local population density (a possible indication of habitat degradation). More generally, habitats in E. f. albocollariss range suffered from fragmentation, reduction in forest area, logging, and potentially greater hunting pressure. Based on these results, it is apparent that more immediate steps are necessary to preserve E. f. albocollaris populations and habitats. Am. J. Primatol. 47:51–60, 1999.

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.

Long-Term Lemur Research at Centre Valbio, Ranomafana National Park, Madagascar

We present findings from 25 years of studying 13 species of sympatric primates at Ranomafana National Park, Madagascar. Long-term studies have revealed that lemur demography at Ranomafana is impacted by climate change, predation from raptors, carnivores, and snakes, as well as habitat disturbance. Breeding is seasonal, and each species (except Eulemur rubriventer) gives birth synchronously to be able to wean before winter. Infant mortality is high (30–70%) and partly due to infanticide in Propithecus edwardsi,and perhaps Varecia variegata. Diurnal lemurs can live beyond 30 years in the wild and most females reproduce until death. Small-bodied Microcebus rufuslive up to 9 years without signs of senescence. Prolemur simusmigrates in search of new bamboo and mates, and related V. variegatamothers park their multiple offspring in “kindergartens,” protected by others while mothers forage. Interference competition among sympatric lemurs occurs. Anthropogenic factors, such as past selective logging and climate change may influence the declining density of E. rufifrons, P. simus, and P. edwardsiwhile not affecting the density of pair-living species.

Aye-aye population genomic analyses highlight an important center of endemism in northern Madagascar

We performed a population genomics study of the aye-aye, a highly specialized nocturnal lemur from Madagascar. Aye-ayes have low population densities and extensive range requirements that could make this flagship species particularly susceptible to extinction. Therefore, knowledge of genetic diversity and differentiation among aye-aye populations is critical for conservation planning. Such information may also advance our general understanding of Malagasy biogeography, as aye-ayes have the largest species distribution of any lemur. We generated and analyzed whole-genome sequence data for 12 aye-ayes from three regions of Madagascar (North, West, and East). We found that the North population is genetically distinct, with strong differentiation from other aye-ayes over relatively short geographic distances. For comparison, the average FST value between the North and East aye-aye populations—separated by only 248 km—is over 2.1-times greater than that observed between human Africans and Europeans. This finding is consistent with prior watershed- and climate-based hypotheses of a center of endemism in northern Madagascar. Taken together, these results suggest a strong and long-term biogeographical barrier to gene flow. Thus, the specific attention that should be directed toward preserving large, contiguous aye-aye habitats in northern Madagascar may also benefit the conservation of other distinct taxonomic units. To help facilitate future ecological- and conservation-motivated population genomic analyses by noncomputational biologists, the analytical toolkit used in this study is available on the Galaxy Web site.

Morphological Variation in Populations of Eulemur albocollaris and E. fulvus rufus

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.

Evolutionary Divergence in the Brown Lemur Species Complex

The brown lemur species group (Eulemur fulvus, E. albocollaris, and E. collaris) is the most widespread of the day-active lemurs, occupying nearly all remaining natural habitats in Madagascar from the extreme north to transitional habitats bordering the arid south, as well as the island of Mayotte in the Comoros (Tattersall, 1982; Mittermeier et al., 1994). The present range in Madagascar is discontinuous, with populations found in coastal and adjacent inland habitats in the north, east, and west (resembling a ring species distribution; Figure 1). However, it is very likely that this vicariance is of recent, anthropogenic origin, as eastern and western populations were once contiguous, occupying the forest mosaics of the high plateau (Tattersall, 1993; Tattersall and Sussman, 1998). In accordance with their wide distribution, brown lemurs demonstrate a high degree of ecological and behavioral flexibility. In this chapter, I will explore their variability and evolutionary divergence, including aspects of morphology, biogeography, ecology, and social systems. In addition, I will summarize the current conservation status of this diverse species complex. Tattersall and Sussman (1998) reviewed the evolution and ecology of brown lemur taxa in the north of Madagascar

Species-level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the worlds most threatened mammals. The critically endangered black-and-white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ∼550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average FST (0.247) and ΦST (0.544), and followed a pattern of isolation-by-distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re-evaluation of conservation management units moving forward.

Predicting Plant Diversity Patterns in Madagascar: Understanding the Effects of Climate and Land Cover Change in a Biodiversity Hotspot

Climate and land cover change are driving a major reorganization of terrestrial biotic communities in tropical ecosystems. In an effort to understand how biodiversity patterns in the tropics will respond to individual and combined effects of these two drivers of environmental change, we use species distribution models (SDMs) calibrated for recent climate and land cover variables and projected to future scenarios to predict changes in diversity patterns in Madagascar. We collected occurrence records for 828 plant genera and 2186 plant species. We developed three scenarios, (i.e., climate only, land cover only and combined climate-land cover) based on recent and future climate and land cover variables. We used this modelling framework to investigate how the impacts of changes to climate and land cover influenced biodiversity across ecoregions and elevation bands. There were large-scale climate- and land cover-driven changes in plant biodiversity across Madagascar, including both losses and gains in diversity. The sharpest declines in biodiversity were projected for the eastern escarpment and high elevation ecosystems. Sharp declines in diversity were driven by the combined climate-land cover scenarios; however, there were subtle, region-specific differences in model outputs for each scenario, where certain regions experienced relatively higher species loss under climate or land cover only models. We strongly caution that predicted future gains in plant diversity will depend on the development and maintenance of dispersal pathways that connect current and future suitable habitats. The forecast for Madagascar’s plant diversity in the face of future environmental change is worrying: regional diversity will continue to decrease in response to the combined effects of climate and land cover change, with habitats such as ericoid thickets and eastern lowland and sub-humid forests particularly vulnerable into the future.