Littoral Forest Fragments Research Articles

Variation in abundance and habitat use of the critically endangered Microcebus gerpi across its fragmented range.

A link between the abundance of species and their degree of ecological specialization has previously been suggested within the primate order. Many species of lemurs were only recently described and even basic ecological data are not yet available for them. We investigated the habitat use, abundance, and habitat characteristics of the critically endangered Microcebus gerpi and evaluated potential impacts of vegetation structure and human disturbances on variations in its abundance. We determined abundance by systematic nocturnal surveys along 13 transects that were also used for characterizing the vegetation structure in seven study sites that were widely distributed within its range. Although M. gerpi occurred in all studied lowland rainforest and littoral forest fragments in central eastern Madagascar and therefore has a higher ecological plasticity and wider distribution than previously thought, its actual Area of Occupancy is very small (339.78 km2 ) due to an extreme degree of habitat fragmentation throughout its range. M. gerpi occurred with a mean encounter rate of 3.04 individuals/km but abundance varied substantially between sites (0.75-4.5 individuals/km). Statistical modeling revealed that the cover of small- to medium-sized trees had a positive impact on the abundance of M. gerpi, whereas a composite disturbance score (CDS), formed on the basis of information on the prominence of fires, cattle, charcoal production and wood extraction inside and around the forest, had a negative impact on abundance. These results suggest that M. gerpi is slightly less threatened than expected because of its larger geographic range, but also that it responds negatively to human disturbances. These findings raise strong conservation concerns and question the long-term viability of the remaining small and isolated populations of this arboreal solitary forager.

Correction to: Population Dynamics of Nocturnal Lemurs in Littoral Forest Fragments: The Importance of Long-Term Monitoring

Correction to: Population Dynamics of Nocturnal Lemurs in Littoral Forest Fragments: The Importance of Long-Term Monitoring

Population Dynamics of Nocturnal Lemurs in Littoral Forest Fragments: The Importance of Long-Term Monitoring

Habitat loss and fragmentation pose a significant threat to many primate species worldwide, yet community-level responses are complex and nuanced. Despite repeated calls from primatologists and the wider conservation community to increase monitoring initiatives that assess long-term population dynamics, such studies remain rare. Here we summarize results from a longitudinal study set in the littoral forests of southeast Madagascar. Littoral forests are a useful model for monitoring lemur population dynamics, as they are relatively well studied and their highly fragmented nature enables the effect of forest size and anthropogenic impacts to be examined. This study focuses on three Endangered nocturnal lemur species—Avahi meridionalis, Cheirogaleus thomasi, and Microcebus tanosi—across three forest fragments of different size and with different usage histories. Between 2011 and 2018, we walked 285 km of line transect and recorded 1968 lemur observations. Based on distance sampling analysis our results indicate that nocturnal lemurs respond to forest patch size and to levels of forest degradation in species-specific ways. The largest species, A. meridionalis, declined in density and encounter rate over time across the three study forests. C. thomasi populations appeared stable in all three fragments, with densities increasing in the most degraded forest. M. tanosi encounter rates were extremely low across all study fragments but were lowest in the most heavily degraded forest fragment. Our results emphasize the importance of localized pressures and species-specific responses on population dynamics. Monitoring population trends can provide an early warning signal of species loss and species-specific responses can inform crucial intervention strategies.

Stuck in fragments: Population genetics of the Endangered collared brown lemur Eulemur collaris in the Malagasy littoral forest.

The Endangered collared brown lemur (Eulemur collaris) is the largest primate living in the littoral forest of southeastern Madagascar, a top priority habitat for biodiversity conservation on the island. Because this lemur is a key seed-disperser, an evaluation of the structure and connectivity of the populations surviving in the forest fragments is urgently needed to guide conservation plans. Genetic variability at autosomal microsatellites and mitochondrial DNA was investigated in a total of 49 collared brown lemurs sampled by non-invasive methods in three littoral forest fragments and in the nearby lowland humid forest. The overall genetic diversity of E. collaris in the southeastern coastal region of Madagascar was lower than in other populations, as well as in other lemur species. The population appears highly structured, with less variable and more inbred groups inhabiting the littoral forest fragments compared to the inland area. Major barriers to gene flow were identified isolating littoral forest fragments from each other and from the inland lowland humid forest. Medium to long-term drift and scarce gene flow is the scenario that best explains the current genetic distribution. Habitat discontinuities such as rivers and grassland between forest fragments played a major role in structuring the population. A common history of size contraction is pointed out by several genetic estimators, indicating a possible ecological crisis triggered around 1,300 years ago. The adoption of strategies aimed at facilitating gene flow and population growth appears crucial to delay further loss of genetic diversity.

Six, not two, species of Acisoma pintail dragonfly (Odonata: Libellulidae).

The dragonfly genus Acisoma is revised based on adult male morphology and COI sequence data. Six species are recognised, including the new species A. attenboroughi sp. nov. Diagnoses and a key to males of all species and illustrations of all relevant characters are provided. A. inflatum, A. variegatum and A. trifidum are confined to continental Africa, while A. panorpoides is restricted to Asia. A. ascalaphoides is known only from threatened littoral forest fragments on the east coast of Madagascar, while A. attenboroughi is widespread across the island. The new species honours Sir David Attenborough on his 90^th birthday.

Habitat corridor utilization by the gray mouse lemur, <i>Microcebus murinus</i>, in the littoral forest fragments of southeastern Madagascar

Habitat fragmentation has reached a dramatic level in Madagascar. As the size of many remaining forest fragments is unlikely to maintain viable animal populations in the long-term, connecting isolated subpopulations by creating corridors is important to support gene flow and the persistence of the endemic fauna, including lemurs. Since restoration with endemic trees is slow, exotic trees may represent a faster alternative to initiate habitats that can be used by animals. Here, we studied whether or not grey mouse lemurs, Microcebus murinus, use corridors composed of exotic and native trees of different age and composition to move between littoral forest fragments. For this, we trapped M. murinus in four forest fragments and mixed tree plantations between the fragments. One of the corridors was composed of a mixture of endemic and mature exotic Eucalyptus robusta trees. The second corridor consisted mainly of an old stand of exotic Melaleuca quinquenervia. The third corridor was composed of exotic Acacia mangium trees planted in 2009. During four years of study, only one male M.murinus used the Melaleuca corridor, while several M. murinus were caught in the Eucalyptus and the Acacia corridor in 2013. The density of the corridor under-story appeared to influence the number of individuals captured; the corridor with highest understory density was used most. The captures within the corridors illustrate that exotic trees allow movements of mouse lemurs within less than 5 years after plantation.

Habitat degradation and seasonality affect physiological stress levels of Eulemur collaris in littoral forest fragments.

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.

A preliminary assessment of nematode infections in Eulemur collaris (Geoffroy, 1812) (Mammalia: Lemuridae) in remnant fragments of Malagasy littoral forest

The rapid rate of habitat loss in Madagascar urges a comprehensive assessment of the threats that its fauna faces by living in fragmented, secondary and/or exotic forests. The role of habitat disturbance in determining potential boosts of parasite infections in lemurs, for instance, has been only recently investigated. Here, we conducted a preliminary assessment of prevalence and intensity of gastrointestinal parasite infections in two populations of endangered red-collared brown lemurs, Eulemur collaris (Geoffroy, 1812) (Mammalia: Lemuridae), living in two littoral forest fragments of southeastern Madagascar. We collected faecal samples from 45 lemurs. The samples were stored in 70% alcohol, and we used a modified McMaster technique to analyze egg shedding. The analysis revealed only nematode infections. We found a higher prevalence of infection in the more disturbed fragment, while no differences were revealed in terms of infection intensity. Prevalence of infection was found to be sex-biased in the less degraded area, being higher in females. We hypothesize that this might have been caused by female immune suppression due to increased energetic costs during pregnancy and/or to avoid possible harm to the foetus. Since red-collared brown lemurs are the largest seed dispersers in the littoral forest and only small populations survive in a few fragments, the implications of our results should be considered in future conservation plans for this habitat.

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments

Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments.

Calumma vohibola, a new chameleon species (Squamata: Chamaeleonidae) from the littoral forests of eastern Madagascar

We describe Calumma vohibola sp. nov., a morphologically distinct chameleon species of the Calumma nasutum species group from littoral forest fragments of the north-central east coast of Madagascar. Males and females of this species differ from all other species of the Calumma nasutum group by an almost absent rostral appendage, by a characteristic stress colouration in the female consisting of a dark reddish ground colouration with many irregular light blue spots, and by significant sequence divergence in the mitochondrial ND2 gene (10.5–19.4% pairwise distance) and no haplotype sharing in the nuclear C-mos gene compared with other members of the C. nasutum group. A molecular survey of C. nasutum populations occurring near the type locality of the new species reveals an extraordinarily high genetic diversity within this morphologically conservative chameleon group. We suspect that C. vohibola might be restricted to a rather small and fragmented distribution range within the last littoral forest fragments along the coast. Owing to the unsolved taxonomic situation of the C. nasutum group, no reliable distribution data of any member of this group are available at present, and hence we cannot ascertain whether the extent of occurrence of C. vohibola is indeed as restricted as suspected. Intensive surveys and field studies are necessary to clarify the distribution limits of this new species and to assess its conservation status reliably.

Ecosystem management in Madagascar during global change

AbstractA long‐held assumption about Madagascar is that all its open vegetation and forest fragments represent anthropogenically degraded landscapes. Further, its forests are believed to lack regenerative capacity following extirpation. This article presents a different ecological framework for southeast Madagascar, a region with diverse forest habitats (humid, littoral, and transitional forests) and exceptional biodiversity. Recently published reconstructions of vegetation change at millennial scales indicate that the mosaic vegetation in southeastern Madagascar represents a natural distribution, with littoral forest spatially constrained by soil moisture, rather than principally fragmented by human activity. There is also evidence that the littoral forest is resilient to climatic change and has acted as refuges and centers of diversification for millennia. By contrast, Uapaca woodlands, which connected the littoral forest fragments, switched to a stable fire‐maintained Ericoid grassland in response to climatic changes. Evidence also suggests that local communities managed forest resources sustainably in the past, but human migration, insecure land tenure, and road expansion may have accelerated forest loss over the last decades. This novel perspective demonstrates the integrated nature of ecological, geomorphological, climatical, and social systems. Finally, combining long‐term with contemporary perspectives, some strategies for maintaining biodiversity under global change, including anthropogenic climate change and mining pressures (and associated biodiversity offset projects) are suggested.

Using nestedness and species-accumulation analyses to strengthen a conservation plan for littoral forest birds in south-eastern Madagascar

The littoral forests of south-eastern Madagascar are among the most threatened ecosystems on the island. A conservation plan has been developed for the region due to a proposed mining venture. Here, we provide a novel methodology to assess if the planned conservation measures would effectively conserve the bird diversity inhabiting these forests. Bird community composition within 30 littoral forest fragments was quantified with each fragment characterized by measures of fragment area, isolation, and internal habitat complexity. A nestedness and cumulative species–area analysis was conducted to ascertain the contribution of forest fragments of different sizes in capturing the overall bird species richness. Datasets representing the overall and forest-dependent bird assemblages were found to be significantly nested. The pattern of nestedness appeared to be driven by fragment size. However, cumulative species–area analyses showed that the assemblages were imperfectly nested with ten species displaying idiosyncratic distribution patterns. When a modest conservation target was set (the occurrence of a bird species in three or more fragments), the proposed conservation plan would only protect approximately half the species found in the littoral forests. We show that protecting an additional four large patches would mean that the proportion of forest-birds captured in three or more patches would increase to 70%. Key words: Madagascar, conservation, littoral forest, mining, fragmentation, nestedness.

Pilot survey of avahi population (woolly lemurs) in littoral forest fragments of southeast Madagascar

This study presents a pilot survey of the avahis (pair-living, nocturnal prosimians) living in threatened littoral forest fragments of southeastern Madagascar. In the period of October-December 2004, I evaluated the density of adult and newborn avahis (carried by the mothers) by counting the individuals encountered during 58 night walks in seven fragments of Sainte Luce and Mandena forests, along one trail/fragment. Along each trail, I used random plots (5 m2) for a preliminary characterization of the vegetation. The density of the population was not correlated with fragment size and number of plant morphospecies, while it was correlated with large tree availability. Possibly due to a low energy diet based on leaves and to specialized and energetically expensive vertical leaping, the loss of large trees by selective logging seems to affect avahi populations more than other variables.

Deforestation and Plant Diversity of Madagascar's Littoral Forests

Few studies have attempted to quantify the reduction or document the floristic composition of forests in Madagascar. Thus, we focused specifically on deforestation and plant diversity in Madagascar's eastern littoral community. We used a data set of approximately 13,500 specimen records compiled from both historical and contemporary collections resulting from recent intensive inventory efforts to enumerate total plant species richness and to analyze the degree of endemism within littoral forests. Change in littoral forest cover from original to current extent was estimated using geographical information systems tools, remote sensing data (satellite imagery and low-elevation digital photography), and environmental data layers. Of the original littoral forest only 10.3% remains in the form of small forest parcels, and only 1.5% of these remaining fragments are included within the existing protected-areas network. Additionally, approximately 13% of Madagascar's total native flora has been recorded from these forests that originally occupied <1% of its total land surface, and over 25% of the 1535 plant species known from littoral forests are endemic to this community. Given the ongoing pressure from human settlement along Madagascar's eastern coast, protection of the remaining forest fragments is critical for their survival. Fifteen of the largest intact littoral forest fragments we identified, collectively representing 41.5% of remaining littoral forest, are among priority sites recommended to the government of Madagascar for plant conservation and incorporation into the protected-areas network.

PARASITE BURDEN AND CONSTITUTION OF MAJOR HISTOCOMPATIBILITY COMPLEX IN THE MALAGASY MOUSE LEMUR, MICROCEBUS MURINUS

We investigated the importance of the major histocompatibility complex (MHC) constitution on the parasite burden of free-ranging mouse lemurs (Microcebus murinus) in four littoral forest fragments in southeastern Madagascar. Fourteen different MHC class II DRB-exon 2 alleles were found in 228 individuals with high levels of sequence divergence between alleles. More nonsynonymous than synonymous substitutions in the functional important antigen recognition and binding sites indicated selection processes maintaining MHC polymorphism. Animals from the four forest fragments differed in their infection status (being infected or not), in the number of different nematode morphotypes per individual (NNI) as well as in the fecal egg counts (FEC) values. Heterozygosity in general was uncorrelated with any of these measures of infection. However, a positive relationship was found between specific alleles and parasite load. Whereas the common allele Mimu-DRB*1 was more frequently found in infected individuals and in individuals with high NNI and FEC values (high parasite load), the rare alleles Mimu-DRB*6 and 10 were more prevalent in uninfected individuals and in individuals with low NNI and FEC values (low parasite load). These three alleles associated with parasite load had unique amino acid motifs in the antigen binding sites. This distinguished them from the remaining 11 Mimu-DRB alleles. Our results support the hypothesis that MHC polymorphism in M. murinus is maintained through pathogen-driven selection acting by frequency-dependent selection. This is the first study of the association of MHC variation and parasite burden in a free-ranging primate.

PARASITE BURDEN AND CONSTITUTION OF MAJOR HISTOCOMPATIBILITY COMPLEX IN THE MALAGASY MOUSE LEMUR, MICROCEBUS MURINUS

We investigated the importance of the major histocompatibility complex (MHC) constitution on the parasite burden of free-ranging mouse lemurs (Microcebus murinus) in four littoral forest fragments in southeastern Madagascar. Fourteen different MHC class II DRB-exon 2 alleles were found in 228 individuals with high levels of sequence divergence between alleles. More nonsynonymous than synonymous substitutions in the functional important antigen recognition and binding sites indicated selection processes maintaining MHC polymorphism. Animals from the four forest fragments differed in their infection status (being infected or not), in the number of different nematode morphotypes per individual (NNI) as well as in the fecal egg counts (FEC) values. Heterozygosity in general was uncorrelated with any of these measures of infection. However, a positive relationship was found between specific alleles and parasite load. Whereas the common allele Mimu-DRB*1 was more frequently found in infected individuals and in individuals with high NNI and FEC values (high parasite load), the rare alleles Mimu-DRB*6 and 10 were more prevalent in uninfected individuals and in individuals with low NNI and FEC values (low parasite load). These three alleles associated with parasite load had unique amino acid motifs in the antigen binding sites. This distinguished them from the remaining 11 Mimu-DRB alleles. Our results support the hypothesis that MHC polymorphism in M. murinus is maintained through pathogen-driven selection acting by frequency-dependent selection. This is the first study of the association of MHC variation and parasite burden in a free-ranging primate.

MHC Variability of a Small Lemur in the Littoral Forest Fragments of Southeastern Madagascar

Habitat fragmentation inhibits gene flow between populations often resulting in a loss of genetic diversity with possible negative effects on fitness parameters. In vertebrates, growing evidence suggests that such genetic diversity is particularly important at the level of the major histocompatibility complex (MHC) because its gene products play an important role in immune functions. Diversity in the MHC is assumed to improve population viability. Here, we investigated the impact of forest fragmentation on the genetic variability of one of the functionally important parts of the MHC, DRB exon 2, of the endemic mouse lemur Microcebus murinus by comparing populations inhabiting two littoral forest fragments of different size in southeastern Madagascar. Twelve different alleles of DRB exon 2 were found in 145 individuals of M. murinus with high levels of sequence divergence between alleles. In both subpopulations, levels of genetic diversity were high, and the genetic analyses revealed only limited effects of fragmentation. Significantly more non-synonymous than synonymous substitutions were found in the functionally important antigen recognition and binding sites indicating selection processes maintaining MHC polymorphism. This is the first study on MHC variation in a free-ranging Malagasy lemur population.

Feeding Ecology ofPteropus rufus(Pteropodidae) in the Littoral Forest of Sainte Luce, SE Madagascar

This paper examines bat-plant interactions by focusing on the fruit diet and food selection of flying foxes (Pteropus rufus) in the littoral forest fragments of Sainte Luce, SE Madagascar. Analyses of faecal samples and opportunistic observations revealed 40 endemic plant species in the diet. The bats mainly eat odorous ripe and juicy berries. No particular fruit colour was predominant in their diet. Both multi- and single-seeded fruits are eaten. Small seeds (1–3.5 mm in length) are usually swallowed whole. Passage through the digestive tract of the flying foxes does not reduce the germination rate of seeds nor the percentage of seeds germinated. This study indicates that the role of flying foxes in both short and long distance seed dispersal for a large number of endemic tree species of the littoral forest should not be underestimated when designing reforestation programs in particular or conservation action plans in general.

Energy Maximizers and Time Minimizers: Theory and Reality

Energy Maximizers and Time Minimizers: Theory and Reality