A preliminary population viability analysis of the critically endangered blue‐eyed black lemur (Eulemur flavifrons)

Population viability analysis is an important tool to assess the extinction risk in small populations of highly specialized primates. The blue‐eyed black lemur (Eulemur flavifrons) is critically endangered with a restricted range in the north‐western dry deciduous forest of Madagascar, where habitat fragmentation and loss of forest connectivity threaten its survival. We performed a population viability analysis (PVA) of this lemur in Ankarafa Forest in the Sahamalaza Peninsula National Park, north‐western Madagascar, to determine the demographic parameters most influential for population persistence and to assess extinction probabilities. We conducted PVA analyses using different demographic parameters which characterize the species including reproduction, lifespan and population size using the software VORTEX for six scenarios with 100 iterations and simulated over 100 years. The simulations suggested the first extinction within 13 years when the percentage of habitat destruction increased up to 12%. Severe habitat destruction such as fire and logging was the major cause which led to the risk of population extinction. Conservation strategies, in particular measures to reduce habitat destruction, are proposed to ensure the survival of this critically endangered lemur.     

Characterization of 21 microsatellite marker loci in the ring-tailed lemur (<Emphasis Type="Italic">Lemur catta</Emphasis>)

Ring-tailed lemur (Lemur catta) is the only species in the Genus Lemur, distributed in the deciduous and spiny forests of southwestern Madagascar. This species is listed as endangered due to the loss and fragmentation of its natural habitat, a consequence of deforestation. Twenty-one nuclear microsatellite loci were isolated from a genomic DNA derived from a free-ranging ring-tailed lemur population from the Tsimanampetsotsa National Park, Madagascar. We report various parameter estimates and measures to establish the utility of this marker suite as screened among individuals this single forest fragment.     

Evolutionary history inferred from the de novo assembly of a nonmodel organism,the blue‐eyed black lemur

Lemurs, the living primates most distantly related to humans, demonstrate incredible diversity in behaviour, life history patterns and adaptive traits. Although many lemur species are endangered within their native Madagascar, there is no high‐quality genome assembly from this taxon, limiting population and conservation genetic studies. One critically endangered lemur is the blue‐eyed black lemur Eulemur flavifrons. This species is fixed for blue irises, a convergent trait that evolved at least four times in primates and was subject to positive selection in humans, where 5′ regulatory variation of OCA2 explains most of the brown/blue eye colour differences. We built a de novo genome assembly for E. flavifrons, providing the most complete lemur genome to date, and a high confidence consensus sequence for close sister species E. macaco, the (brown‐eyed) black lemur. From diversity and divergence patterns across the genomes, we estimated a recent split time of the two species (160 Kya) and temporal fluctuations in effective population sizes that accord with known environmental changes. By looking for regions of unusually low diversity, we identified potential signals of directional selection in E. flavifrons at MITF, a melanocyte development gene that regulates OCA2 and has previously been associated with variation in human iris colour, as well as at several other genes involved in melanin biosynthesis in mammals. Our study thus illustrates how whole‐genome sequencing of a few individuals can illuminate the demographic and selection history of nonmodel species.     

Climate change and human colonization triggered habitat loss and fragmentation in Madagascar

The relative effect of past climate fluctuations and anthropogenic activities on current biome distribution is subject to increasing attention, notably in biodiversity hot spots. In Madagascar, where humans arrived in the last ~4 to 5,000 years, the exact causes of the demise of large vertebrates that cohabited with humans are yet unclear. The prevailing narrative holds that Madagascar was covered with forest before human arrival and that the expansion of grasslands was the result of human‐driven deforestation. However, recent studies have shown that vegetation and fauna structure substantially fluctuated during the Holocene. Here, we study the Holocene history of habitat fragmentation in the north of Madagascar using a population genetics approach. To do so, we infer the demographic history of two northern Madagascar neighbouring, congeneric and critically endangered forest dwelling lemur species—Propithecus tattersalli and Propithecus perrieri—using population genetic analyses. Our results highlight the necessity to consider population structure and changes in connectivity in demographic history inferences. We show that both species underwent demographic fluctuations which most likely occurred after the mid‐Holocene transition. While mid‐Holocene climate change probably triggered major demographic changes in the two lemur species range and connectivity, human settlements that expanded over the last four millennia in northern Madagascar likely played a role in the loss and fragmentation of the forest cover.     

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

Lemurs are among the world's 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 F_ST (0.247) and Φ_ST (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.     

Ecosystem engineers maintain a rare species of butterfly and increase plant diversity

We evaluated whether ecosystem engineers can accomplish two conservation goals simultaneously: (1) indirectly maintain populations of an endangered animal through habitat modification and (2) increase riparian plant diversity. We tested for effects of a prominent ecosystem engineer, the beaver Castor canadensis, on populations of St. Francis' satyr butterfly Neonympha mitchellii francisci and plant species richness and composition. We performed our test by surveying riparian vegetation communities in all stages of beaver‐influenced wetland succession. We found that beavers created wetland habitats that supported plant species not found elsewhere in riparian zones and increased plant species diversity across the landscape by creating a novel combination of patch types. Our results confirmed what others have found about engineering effects on plant diversity, but these results further demonstrated a case where ecosystem engineers indirectly maintain populations of rare animals by modifying the composition and diversity of plant communities within wetlands. Our research demonstrates how an ecosystem engineer can influence habitat availability and composition of plant communities important for an endangered insect, and maintain overall plant species diversity by increasing habitat heterogeneity.     

Population Status and Reproductive Success of an Endangered Epiphytic Orchid in a Fragmented Landscape

Habitat fragmentation and disturbance are two of the most significant drivers of species extinctions in plant populations. The degree of impact of fragmentation on plant populations depends on the level of specificity of plant–animal interactions, as well as on the availability of suitable sites for seedling recruitment. In this study, we describe the population density and structure, pollen limitation and reproductive success of the endangered tropical orchid Myrmecophila christinae, an epiphytic species with a specialized pollination system. We surveyed a total of 14 populations located in a fragmented landscape. Seedling density was related to habitat disturbance and host plant density; while density of juveniles was related to density of adults. Adult and total individual densities were related to habitat affectation. We also found that fragments <1 ha had significantly fewer seedlings, as well as an over‐representation of large adults. On the other hand, fruit production was higher in fragments >10 ha, and fruit set was significantly lower in highly disturbed fragments. Hand pollination experiments showed that M. christinae was pollen limited in all the studied populations, suggesting that pollen limitation is unrelated to habitat disturbance. Overall, our results suggest that fragmentation has affected key demographic features of M. christinae, including reproduction and recruitment.     

Assessing Extinction Risk in Small Metapopulations of Golden‐headed Lion Tamarins (Leontopithecus chrysomelas) in Bahia State,Brazil

Golden‐headed lion tamarins (GHLTs; Leontopithecus chrysomelas) are endangered primates endemic to the Brazilian Atlantic Forest, where loss of forest and its connectivity threaten species survival. Understanding the role of habitat availability and configuration on population declines is critical for guiding proactive conservation for this, and other, endangered species. We conducted population viability analysis to assess vulnerability of ten GHLT metapopulations to habitat loss and small population size. Seven metapopulations had a low risk of extirpation (or local extinction) over the next 100 years assuming no further forest loss, and even small populations could persist with immediate protection. Three metapopulations had a moderate/high risk of extirpation, suggesting extinction debt may be evident in parts of the species’ range. When deforestation was assumed to continue at current rates, extirpation risk significantly increased while abundance and genetic diversity decreased for all metapopulations. Extirpation risk was significantly negatively correlated with the size of the largest patch available to metapopulations, underscoring the importance of large habitat patches for species persistence. Finally, we conducted sensitivity analysis using logistic regression, and our results showed that local extinction risk was sensitive to percentage of females breeding, adult female mortality, and dispersal rate and survival; conservation or research programs that target these aspects of the species’ biology/ecology could have a disproportionately important impact on species survival. We stress that efforts to protect populations and tracts of habitat of sufficient size throughout the species’ distribution will be important in the near‐term to protect the species from continuing decline and extinction.     

Species‐area relationships of lemurs in a fragmented landscape in Madagascar

We used species‐area relationships (SARs) to investigate the effects of habitat loss on lemur biogeography. We measured species richness via visual surveys on line transects within 42 fragments of dry deciduous forest at the Ambanjabe field site in Ankarafantsika National Park, Madagascar. We measured human disturbance and habitat characteristics within 38 of the 42 fragments. We measured the distance between each fragment and the nearest settlement, continuous forest, and nearest neighboring fragment. We fit 10 candidate SAR models to the data using nonlinear least squares regression and compared them using Akaike's Information Criterion (AIC). To determine how habitat characteristics, as well as area, influenced species richness, we ran a hierarchical partitioning procedure to select which variables to include in generalized additive models (GAMs) and compared them using AIC. Contrary to expectations, we found that lemurs form convex SARs, without a “small island effect”, and with the power model being the most likely SAR model. Although we found that four variables (area, survey effort, and total human disturbance, and mean tree height) independently contributed greater than 10% of the variation in lemur species richness, only area was included in the most likely model. We suggest that the power model was the most likely SAR model and our inability to detect a “small island effect” are the result of Microcebus spp. being edge tolerant and capable of dispersing through matrix, scale issues in the study design, and low γ‐diversity in the landscape. However, more study is needed to determine what role human disturbance plays in influencing species richness in lemurs.     

Ant Diversity in Dominant Vegetation Types of Southern Cameroon

Ants have been shown as particularly affected by land disturbance through deforestation and conversion of forest to agriculture. The effect of land use change on ant diversity in the Congo Basin is not well known. We conducted intensive sampling along a gradient of increasing vegetation disturbance to test the effect of habitat disturbance on ant diversity and Functional Groups composition. Sampling was conducted in 30 plots (5 study sites × 3 habitat × 2 plots/habitat), replicated six times in 1 year. In each plot, ants were monitored with pitfall traps, quadrats and baits. We recorded 237 ant morphospecies grouped in 10 subfamilies and 43 genera. Myrmicaria opaciventris was the most abundant species followed by Anoplolepis tenella. Forest had greater ant diversity compared with fallows and mixed‐crop fields. Functional groups were dominated by Opportunists, followed by Omnivorous Arboreal Dominants and Generalized Mymicinae. Their composition was not affected by the disturbance, but occurrence of Specialist Predators decreased with increasing disturbance. Occurrence of Generalized Myrmicinae, Opportunists and Subordinate Camponotini increased with disturbance. These results indicate that forest conversion into mixed‐crop fields reduce ant diversity. It can also increase abundance of species with generalized diet that predominates where stress and disturbance limits other ants.     

Effects of anthropogenic disturbance on indri (Indri indri) health in Madagascar

Anthropogenic habitat disturbance impairs ecosystem health by fragmenting forested areas, introducing environmental contamination, and reducing the quality of habitat resources. The effect of this disturbance on wildlife health is of particular concern in Madagascar, one of the world's biodiversity hotspots, where anthropogenic pressures on the environment remain high. Despite the conservation importance of threatened lemur populations in Madagascar, few data exist on the effects of anthropogenic disturbance on lemur health. To examine these impacts, indri (Indri indri) populations were evaluated from two forest reserves that differ in their exposure to anthropogenic disturbance. We compared the health status of 36 indri individuals from two sites: one population from a protected, undisturbed area of lowland evergreen humid forest and the other population from a reserve exposed to frequent tourism and forest degradation. Comparison of indri health parameters between sites suggests an impact of anthropogenic disturbance, including significant differences in leukocyte count and differential, 12 serum parameters, 6 trace minerals, and a higher diversity of parasites, with a significant difference in the presence of the louse, Trichophilopterus babakotophilus. These data suggest that indri living in disturbed forests may experience physiological changes and increased susceptibility to parasitism, which may ultimately impair reproductive success and survival.     

The cascading effects of elephant presence/absence on arthropods and an Afrotropical thrush in Arabuko‐Sokoke Forest,Kenya

Although studies have explored how habitat structure and disturbance affect arthropod communities, few have explicitly tested the effects of both structure and disturbance level across trophic levels and phyla. We present here the results of a study conducted in the Arabuko‐Sokoke Forest (ASF) of coastal Kenya, in which abundance of arthropods and one of their avian predators, the East Coast Akalat Sheppardia gunning sokokensis was compared in relatively undisturbed habitat (outside elephant roaming areas) and in disturbed habitat (inside elephant roaming areas). Vegetation structure in both areas was measured using several metrics, including leaf litter depth, understory vegetation density, animal disturbance and fallen log counts. Leaf litter and coleopteran abundance were higher outside the elephant roaming areas, whereas understory visibility, animal disturbance and dipteran diversity were much higher inside the elephant areas. Species composition of several arthropod taxa (e.g. Hymenoptera, Coleoptera, Diptera, Hemiptera and Araneae) was also influenced by degree of disturbance, whereas akalat abundance was inversely related to understory visibility. Our results suggest that differences in species sensitivity to habitat disturbance and vegetation structure across trophic levels should be incorporated into the management and conservation of rare and endangered species.     

Impact of pocket gopher disturbance on plant species diversity in a shortgrass prairie community

Summary We examined the impact of pocket gopher disturbances on the dynamics of a shortgrass prairie community. Through their burrowing activity, pocket gophers (Thomomys bottae) cast up mounds of soil which both kill existing vegetation and create sites for colonization by competitively-inferior plant species. Three major patterns emerge from these disturbances: First, we show that 10 of the most common herbaceous perennial dicots benefit from pocket gopher disturbance; that is, a greater proportion of seedlings are found in the open space created by pocket gopher disturbance than would be expected based on the availability of disturbed habitat. Additionally, these seedlings exhibited higher growth rates than adjacent seedlings of the same species growing in undisturbed habitat. Second, we tested two predictions of the Intermediate Disturbance Hypothesis and found that species diversity was greatest for plots characterized by disturbances of intermediate age. However, we did not detect significant differences in diversity between plots characterized by intermediate and high levels of disturbance, indicating that many species are adapted to or at least tolerant of high levels of disturbance. Third, we noted that the abundance of grasses decreased with increasing disturbance, while the abundance of dicots increased with increasing disturbance.     

Characterization of 21 microsatellite marker loci in the Milne-Edwards’ Sifaka (Propithecus edwardsi)

Milne-Edwards’ Sifaka (Propithecus edwardsi) is a dark furred lemur with white flanks living in the southern region of the eastern rainforest belt of Madagascar. This species is endangered due to habitat destruction primarily from deforestation. Twenty-one polymorphic nuclear microsatellite loci were isolated from a genomic DNA derived from an individual from Ranomafana National Park, Madagascar. Population genetic parameters were estimated on 10 individuals each, from Andringitra National Park and the Vatoharana Forest in Ranomafana National Park.     

Effects of anthropogenic habitat disturbance and Giardia duodenalis infection on a sentinel species' gut bacteria

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human–animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host–microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host–microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals.     

Genetic variability and the effect of habitat fragmentation in spotted suslik Spermophilus suslicus populations from two different regions

Endangered species worldwide exist in remnant populations, often within fragmented landscapes. Although assessment of genetic diversity in fragmented habitats is very important for conservation purposes, it is usually impossible to evaluate the amount of diversity that has actually been lost. Here, we compared population structure and levels of genetic diversity within populations of spotted suslik Spermophilus suslicus, inhabiting two different parts of the species range characterized by different levels of habitat connectivity. We used microsatellites to analyze 10 critically endangered populations located at the western part of the range, where suslik habitat have been severely devastated due to agriculture industrialization. Their genetic composition was compared with four populations from the eastern part of the range where the species still occupies habitat with reasonable levels of connectivity. In the western region, we detected extreme population structure (F _ST = 0.20) and levels of genetic diversity (Allelic richness ranged from 1.45 to 3.07) characteristic for highly endangered populations. Alternatively, in the eastern region we found significantly higher allelic richness (from 5.09 to 5.81) and insignificant population structure (F _ST = 0.03). As we identified a strong correlation between genetic and geographic distance and a lack of private alleles in the western region, we conclude that extreme population structure and lower genetic diversity is due to recent habitat loss. Results from this study provide guidelines for conservation and management of this highly endangered species.     

A Meta-Analysis of the Impact of Anthropogenic Forest Disturbance on Southeast Asia's Biotas

The impacts of tropical deforestation and forest degradation on SE Asia's biotas have been documented, but a quantitative synthesis is currently lacking. We examined the responses of biodiversity to anthropogenic forest disturbance by comparing key ecological attributes between undisturbed and neighboring disturbed forests. Based on data from four taxonomic groups (vascular plants, invertebrates, birds, and mammals), six broad measures of 'ecological health' ( e.g. , richness, abundance, and demographics), and a range of different impact types from 120 articles published, we calculated the proportion of pairwise comparisons in which the measure of ecological health was lower in impacted than in pristine sites, as would be expected if forest disturbance was detrimental. The explanatory power of correlates of disturbance sensitivity was assessed using an information-theoretic evaluation of a candidate set of generalized linear models (GLMs). Overall, 73.6 percent (95% CI = 70.8–76.2%) of 1074 pairwise comparisons supported the expectation that forest disturbance was detrimental to ecological health, with mammals being the most sensitive group. The median effect size was for pristine areas to have 22.2 percent higher ecological health than equivalent disturbed areas. The most responsive measure of ecological health was species richness (median = 28.6% higher in pristine), and agricultural areas were the most ecologically degraded (median = 35.6% higher in pristine). However, the GLMs revealed no marked differences overall between taxonomic groups, habitat impact types, or ecological health measures. Our finding implies that the sensitivity of biodiversity to forest disturbance is moderately high, but essentially universal, suggesting urgent forest conservation actions.     

More species,but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity

The role of habitat disturbance on biodiversity is central as it promotes changes in ecological systems. That said, still little is known about the functional consequences of such changes. Functional diversity can be used to revealing more mechanistically the disturbance effects on communities by considering the richness and the distribution of traits among the species. Here we analyzed the response of functional and species diversity of ground beetles to flood disturbance to better understand the functioning of alluvial invertebrate communities. Ground beetles were sampled in periodically flooded grasslands along the Elbe River in Germany. We used generalized linear mixed effects models to unveil the relationships between flood disturbance, species and functional diversity, respectively. We measured different components of functional diversity (functional richness, evenness, dispersion, and divergence) and analyzed species diversity by means of rarefied species richness, abundances, evenness and Simpson's diversity. We found contrasting relationships in that most species diversity measures peaked at highest disturbance levels, while most functional diversity measures decreased with increasing disturbance intensities. Inversed relationships between species and functional diversity are rarely observed, as most studies report on positive correlations. We explain increasing species diversity with a higher amount of resources available in highly disturbed sites. Decreasing functional diversity is best explained through the convergence of species traits by flood disturbance and uneven resource exploitation in highly disturbed plots (low functional evenness), suggesting strong impacts from functionally different generalist species in floodchannels. We show that the amount of resources available, and how these resources are exploited, play major roles in the functioning of floodplain ground beetle communities.     

Long-term genetic monitoring of a translocated population of collared brown lemurs

Post-release monitoring is important to improve translocation success because it provides an opportunity to identify factors relevant to the survival of local populations. We studied a population of the endangered collared brown lemur (Eulemur collaris) translocated from a degraded forest fragment to a nearby littoral forest within the Mandena Conservation Area in southeast Madagascar from 2000–2011. We compared genetic surveys of mitochondrial and nuclear markers with the genetic profile of nearby populations to examine the dispersal capacity of the collared brown lemur. We also performed a landscape analysis to assess changes in connectivity between forest fragments. There was a fluctuating trend characterized by a phase of demographic and genetic stability shortly after translocation, followed by an increase in genetic diversity coinciding with a population decrease and a gradual recovery of initial conditions. These results demonstrated the ability of the collared brown lemur to disperse through unfavorable landscapes and to recover after translocation. Our study revealed the importance of monitoring translocated populations over time using a multidisciplinary approach.     

Characterization of 13 microsatellite marker loci in Verreaux's sifaka (Propithecus verreauxi)

The Verreaux's sifaka (Propithecus verreauxi) is one of the species of Propithecus, living in the dry forest of southwest Madagascar. This species is endangered due to the loss and fragmentation of its natural habitat, a consequence of deforestation. Thirteen novel nuclear microsatellite loci were isolated and characterized in three populations of Verreaux's sifaka. The marker suite proved informative with an average of 8.9 alleles per locus and observed heterozygosity across the three populations of 0.675.