Microcebus Ravelobensis Research Articles

Temporal dynamics in gastrointestinal helminth infections of sympatric mouse lemur species (Microcebus murinus and Microcebus ravelobensis) in Northwestern Madagascar

Madagascar's lemur populations are declining in dwindling habitats due to anthropogenic expansion and changing climatic conditions. Gastrointestinal parasites can be important indicators to assess the health status of threatened species. However, parasites, hosts and the environment are connected in complex interactions. The present study aimed to disentangle the impact of seasonal and several host-specific factors (sex, species, age, reproductive status, and body mass) on endoparasitism in two small-bodied, co-occurring lemur species (Microcebus murinus and Microcebus ravelobensis) in the Ankarafantsika National Park. Helminth prevalence and egg shedding intensity was investigated via copromicroscopic examination of 810 fecal samples that were obtained from 178 individuals across an 11-month period with a longitudinal approach via repeated captures in a 30.6 ha forest area. Both mouse lemur hosts shed seven morphologically distinct egg types (assigned to Subulura baeri, unidentified Enterobiinae, Spirura sp., Lemuricola sp., two Hymenolepididae spp., one unidentified ascarid). Postmortem examination of two deceased individuals enabled assignment of adult worms to egg morphotypes of S. baeri, Spirura sp. and one Hymenolepididae sp., supported by molecular analysis. A significant seasonal variation was observed in the occurrence of the three most common helminth species S. baeri (total prevalence 71%), unidentified Enterobiinae (46%) and Spirura sp. (38%), with a higher likelihood of infection with advancing dry season. Neither host species, sex nor reproductive status had a significant effect on gastrointestinal helminth infections. Host body mass showed pronounced seasonal changes but did not differ significantly between infected and non-infected individuals. The pathogenic effects of gastrointestinal helminths therefore likely remained within compensable limits in the studied mouse lemur populations. Our findings highlight the prominent influence of seasonal changes on helminth communities. The results of combined morphologic and genetic approaches can furthermore help to overcome limitations of parasite identification via copromicroscopy by linking egg morphology to DNA sequences.

Where the small things are: Modelling edge effects on mouse lemur population density and distribution in northwestern Madagascar.

Edge effects result from the penetration to varying depths and intensities, of abiotic and biotic conditions from the surrounding non-forest matrix into the forest interior. Although 70% of the world's forests are within 1 km of a forest edge, making edge effects a dominant feature of most forest habitats, there are few empirical data on inter-site differences in edge responses in primates. We used spatially explicit capture-recapture (SECR) models to determine spatial patterns of density for two species of mouse lemurs (Microcebus murinus and Microcebus ravelobensis) in two forest landscapes in northwestern Madagascar. The goal of our study was to determine if mouse lemurs displayed spatially variable responses to edge effects. We trapped animals using Sherman live traps in the Mariarano Classified Forest (MCF) and in the Ambanjabe Forest Fragment Site (AFFS) site within Ankarafantsika National Park. We trapped 126 M. murinus and 79 M. ravelobensis at MCF and 78 M. murinus and 308 M. ravelobensis at AFFS. For M. murinus, our top model predicted a positive edge response, where density increased towards edge habitats. In M. ravelobensis, our top model predicted a negative edge response, where density was lower near the forest edges and increased towards the forest interior. At regional and landscape-specific scales, SECR models estimated different density patterns between M. murinus and M. ravelobensis as a result of variation in edge distance. The spatial variability of our results using SECR models indicate the importance of studying the population ecology of primates at varying scales that are appropriate to the processes of interest. Our results lend further support to the theory that some lemurs exhibit a form of ecological flexibility in their responses to forest loss, forest fragmentation, and associated edge effects.

Host-related and environmental factors influence long-term ectoparasite infestation dynamics of mouse lemurs in northwestern Madagascar.

Parasite infestations depend on multiple host-related and environmental factors. In the case of ectoparasites, which are exposed to the environment beyond the host, an impact of climate, expressed by seasonal or yearly variations, can be expected. However, long-term dynamics of ectoparasite infestations are rarely studied in nonhuman primates. We investigated the yearly variations in ectoparasite infestations of two small primates, the gray (Microcebus murinus) and the golden-brown (Microcebus ravelobensis) mouse lemur. For a more comprehensive evaluation, we also analyzed the potential effects of yearly and monthly climatic variation (temperature, rainfall) in addition to habitat, host sex, age, species, and body mass, on ectoparasite infestation. Individuals of both host species were sampled in two study sites within the Ankarafantsika National Park in northwestern Madagascar during several months (March-November) and across 4 years (2010, 2011, 2015, 2016). Our results show significant monthly and yearly variations in the infestation rates of three native ectoparasite taxa (Haemaphysalis spp. ticks, Schoutedenichia microcebi chigger mites, Lemurpediculus spp. sucking lice) and in ectoparasite species richness in both mouse lemur species. In addition, significant impacts of several host-related (species, sex, body mass) and environmental factors (habitat, temperature, rainfall) were found, but with differences in relevance for the different parasite taxa and partly deviating in their direction. Although some differences could be attributed to either permanent or temporary presence of the parasites on the host or to ecological differences between the host species, the lack of specific knowledge regarding the life cycle and microhabitat requirements of each parasite taxon precludes a complete understanding of the factors that determine their infestation dynamics. This study demonstrates the presence of yearly and monthly dynamics in lemur-parasite interactions in tropical, seasonal, dry deciduous forests in Madagascar, which call out for broad ecological long-term studies focusing both on primate hosts and their parasites.

Molecular phylogenetics of the sucking louse genus Lemurpediculus (Insecta: Phthiraptera), ectoparasites of lemurs, with descriptions of three new species.

Sucking lice live in intimate association with their hosts and often display a high degree of host specificity. The present study investigated sucking lice of the genus Lemurpediculus from six mouse lemur (Microcebus) and two dwarf lemur (Cheirogaleus) species endemic to the island of Madagascar, considered a biodiversity hotspot. Louse phylogenetic trees were created based on cytochrome C oxidase subunit I (COI), elongation factor 1α (EF1α) and internal transcribed spacer 1 (ITS1) sequences. While clustering according to host species was generally observed for COI and ITS1, suggesting high host specificity of the examined lice, EF1α sequences alone did not distinguish between lice of different Microcebus species, possibly due to rather recent divergence. As bootstrap support for basal tree structure was rather low, further data are necessary to resolve the evolutionary history of louse-mouse lemur associations. Three new species of sucking lice are described: Lemurpediculus zimmermanni sp. Nov. From Microcebus ravelobensis, Lemurpediculus gerpi sp.nov. from Microcebus gerpi, and Lemurpediculus tsimanampesotsae sp. nov. from Microcebus griseorufus. These new species are compared with all known congeneric species and identifying features are illustrated for all known species of Lemurpediculus.

Filarial infections in lemurs:Evidence for a wide geographical distribution and low host specificity among lemur species.

The relevance of emerging infectious diseases continues to grow worldwide as human activities increasingly extend into formerly remote natural areas. This is particularly noticeable on the island of Madagascar. As closest relatives to humans on the island, lemurs are of particular relevance as a potential origin of zoonotic pathogen spillover. Knowledge of pathogens circulating in lemur populations is, however, very poor. Particularly little is known about lemur hemoparasites. To infer host range, ecological and geographic spread of the recently described hemoparasitic nematode Lemurfilaria lemuris in northwestern Madagascar, a total of 942 individuals of two mouse lemur species (Microcebus murinus [n = 207] and Microcebus ravelobensis [n = 433]) and two rodent species (the endemic Eliurus myoxinus [n = 118] and the invasive Rattus rattus [n = 184]) were captured in two fragmented forest landscapes (Ankarafantsika National Park and Mariarano Classified Forest) in northwestern Madagascar for blood sample examination. No protozoan hemoparasites were detected by microscopic blood smear screening. Microfilaria were present in 1.0% (2/207) of M. murinus and 2.1% (9/433) of M. ravelobensis blood samples but not in rodent samples. Internal transcribed spacer 1 (ITS-1) sequences were identical to an unnamed Onchocercidae species previously described to infect a larger lemur species, Propithecus verreauxi, about 650 km further south. In contrast to expectations, L. lemuris was not detected. The finding of a pathogen in a distantly related host species, at a considerable geographic distance from the location of its original detection, instead of a microfilaria species previously described for one of the studied host species in the same region, illustrates our low level of knowledge of lemur hemoparasites, their host ranges, distribution, modes of transmission, and their zoonotic potential. Our findings shall stimulate new research that will be of relevance for both conservation medicine and human epidemiology.

RADseq Data Suggest Occasional Hybridization between Microcebus murinus and M. ravelobensis in Northwestern Madagascar.

The occurrence of natural hybridization has been reported in a wide range of organisms, including primates. The present study focuses on the endemic lemurs of Madagascar, primates for which only a few species occur in sympatry or parapatry with congeners, thereby creating limited opportunity for natural hybridization. This study examines RADseq data from 480 individuals to investigate whether the recent expansion of Microcebus murinus towards the northwest and subsequent secondary contact with Microcebus ravelobensis has resulted in the occurrence of hybridization between the two species. Admixture analysis identified one individual with 26% of nuclear admixture, which may correspond to an F2- or F3-hybrid. A composite-likelihood approach was subsequently used to test the fit of alternative phylogeographic scenarios to the genomic data and to date introgression. The simulations yielded support for low levels of gene flow (2Nm0 = 0.063) between the two species starting before the Last Glacial Maximum (between 54 and 142 kyr). Since M. murinus most likely colonized northwestern Madagascar during the Late Pleistocene, the rather recent secondary contact with M. ravelobensis has likely created the opportunity for occasional hybridization. Although reproductive isolation between these distantly related congeners is not complete, it is effective in maintaining species boundaries.

Consumption of insect and plant exudates by mouse lemurs

While exploring Isalo National Park in southcentral Madagascar, we observed numerous nymphs and adults of the endemic flatid leaf bug (Phromnia rosea). As in many other hemipterans (including aphids, scale insects, and leafhoppers), nymphs of these leaf bugs feed on phloem and expel a liquid endearingly termed “honeydew” from their anuses. This sugary substance drops onto leaves and stems. In northwestern Madagascar, the gray mouse lemur (Microcebus murinus), golden-brown mouse lemur (Microcebus ravelobensis), Madame Berthe’s mouse lemur (Microcebus berthae, the world’s smallest primate, found only in a small area in western Madagascar), and ring-tailed lemur (Lemur catta, which are in a different family from the others) mostly consume honeydew and plant-based exudates such as gums during the dry season. Honeydew could be a critical resource during periods of food scarcity (Joly-Radko and Zimmerman 2010; doi.org/10.1007/978-1-4419-6661-2_7), and lemurs are the only mammals ever documented to eat honeydew. Precious little is known about most of the mouse lemurs, and until the late 20th century only one species was recognized – now, more than 20 are known. However, collecting field data on flatid leaf bugs and mouse lemurs is challenging. Future studies could determine whether exudates account for a substantial fraction of their calories in the dry season, and if dietary shifts are accompanied by changes in the lemurs’ gut microbiota.

Enter the Matrix: Use of Secondary Matrix by Mouse Lemurs

Madagascar is home to many threatened and endemic primate species, yet this island has seen dramatic declines in lemur habitat due to forest loss. This forest loss has resulted in an increasingly fragmented forest landscape, with fragments isolated from each other by grasslands (i.e., matrix). The grassland matrix is not entirely homogeneous containing matrix elements such as isolated trees and shrubs and linear features such as drainage lines. Because most lemurs are predominantly arboreal, they may preferentially use matrix elements to facilitate dispersal between fragments for access to mates or reduce feeding competition, allowing gene flow between fragments of habitat. Therefore, it is important to understand to what degree they use the matrix. We investigated matrix use in two mouse lemurs, the grey mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (Microcebus ravelobensis) in a fragmented landscape in northwest Madagascar. We tested the predictions that: (1) lemurs use matrix less often than forest fragments, (2) if they use the matrix, then they will preferentially use matrix elements compared to grassland, and (3) M. murinus will disperse into the matrix further than M. ravelobensis. In 2011, we visually surveyed line transects in four areas containing matrix elements and four adjacent forest fragments during nocturnal walks. In 2017, we set up traplines in four areas of the matrix containing matrix elements, three areas that were grassland, and six traplines in adjacent fragments. We compared the relative abundance of mouse lemurs in matrix transects to fragmented forest transects, and the relative abundance of captured lemurs in matrix elements, grassland, and fragment traplines. We found that encounter rates of mouse lemurs did not significantly differ between the matrix and fragmented forest transects or traplines. Our sample size was too low to determine if the mean distance from the forest was greater for either Microcebus spp. Our study highlights that mouse lemurs do use matrix elements and there may be interspecific differences in use. Further research is needed to confirm species-specific matrix use, why mouse lemurs use matrix, and how much matrix elements facilitate movement for each species in fragmented landscapes.

Effects of habitat edges on vegetation structure and the vulnerable golden-brown mouse lemur (Microcebus ravelobensis) in northwestern Madagascar

BackgroundEdge effects can influence species composition and community structure as a result of changes in microenvironment and edaphic variables. We investigated effects of habitat edges on vegetation structure, abundance and body mass of one vulnerable Microcebus species in northwestern Madagascar. We trapped mouse lemurs along four 1000-m transects (total of 2424 trap nights) that ran perpendicular to the forest edge. We installed 16 pairs of 20 m2 vegetation plots along each transect and measured nine vegetation parameters. To determine the responses of the vegetation and animals to an increasing distance to the edge, we tested the fit of four alternative mathematical functions (linear, power, logistic and unimodal) to the data and derived the depth of edge influence (DEI) for all parameters.ResultsLogistic and unimodal functions best explained edge responses of vegetation parameters, and the logistic function performed best for abundance and body mass of M. ravelobensis. The DEI varied between 50 m (no. of seedlings, no. of liana, dbh of large trees [dbh ≥ 10 cm]) and 460 m (tree height of large trees) for the vegetation parameters, whereas it was 340 m for M. ravelobensis abundance and 390 m for body mass, corresponding best to the DEI of small tree [dbh < 10 cm] density (360 m). Small trees were significantly taller and the density of seedlings was higher in the interior than in the edge habitat. However, there was no significant difference in M. ravelobensis abundance and body mass between interior and edge habitats, suggesting that M. ravelobensis did not show a strong edge response in the study region. Finally, regression analyses revealed three negative (species abundance and three vegetation parameters) and two positive relationships (body mass and two vegetation parameters), suggesting an impact of vegetation structure on M. ravelobensis which may be partly independent of edge effects.ConclusionsA comparison of our results with previous findings reveals that edge effects are variable in space in a small nocturnal primate from Madagascar. Such an ecological plasticity could be extremely relevant for mitigating species responses to habitat loss and anthropogenic disturbances.

Forest edges affect ectoparasite infestation patterns of small mammalian hosts in fragmented forests in Madagascar

Habitat loss and fragmentation drive the worldwide depletion of biodiversity. Although it is known that anthropogenic disturbances severely affect host and ecosystem integrity, effects on parasites are largely understudied. This study aims to investigate if and how habitat fragmentation affects the composition of ectoparasite communities on small mammalian hosts in two networks of dry deciduous forest fragments in northwestern Madagascar. Forest sites differing in size, proportion of edge habitat and host density were studied in the Ankarafantsika National Park and in the Mariarano region. A total of 924 individuals of two mouse lemur species, Microcebus murinus (n = 200) and Microcebus ravelobensis (n = 426), and two rodent species, endemic Eliurus myoxinus (n = 114) and introduced Rattus rattus (n = 184), were captured to assess ectoparasite infestations. Ectoparasite prevalence and ectoparasite species richness were statistically related to nine ecological variables applying generalized linear mixed models. Hosts harbored ticks (Haemaphysalis microcebi), mites (Schoutedenichia microcebi, Listrophoroides spp., Laelaptidae gen. spp.) and sucking lice (Lemurpediculus spp., Polyplax sp., Hoplopleuridae gen. sp.). Parasite prevalence differed significantly between host species for all detected parasite taxa. Proximity to the forest edge led to a significant reduction in ectoparasites. Parasite-specific edge effects were observed up to a distance of 750 m from the forest edge. The obtained results imply that habitat fragmentation impacts ectoparasite communities, in particular by negatively affecting temporary parasite species. The results are best explained by an interplay of parasite life cycles, responses to changes in abiotic factors induced by edges and host-specific responses to habitat fragmentation. The negative responses of most studied ectoparasite taxa to forest edges and habitat fragmentation demonstrate their ecological vulnerability that may eventually threaten the integrity of ecosystems and potentially impact ectoparasite biodiversity worldwide.

Ecological fragmentation effects in mouse lemurs and small mammals in northwestern Madagascar.

Habitat loss and fragmentation are major ecological forces threatening animal communities across the globe. These issues are especially true in Madagascar, where forest loss is ongoing. We examined the effects of forest fragmentation on the distribution and abundance of sympatric, endemic gray, and golden-brown mouse lemurs (Microcebus murinus and Microcebus ravelobensis), the endemic western tuft-tailed rat (Eliurus myoxinus), and the invasive black rat (Rattus rattus) in two regions in northwestern Madagascar. We used systematic capture procedures in 40 forest fragments and four continuous forest sites which differed in size, shape, and degree of isolation. With a trapping effort of 11,567 trap nights during two dry seasons (2017-2018), we captured 929 individuals (432 M. ravelobensis, 196 M. murinus, 116 E. myoxinus, and 185 R. rattus). We examined the influence of study region, forest type (fragment vs. continuous), forest size, forest shape, the proportion of 50-m forest edge and distance to continuous forest on the abundance and interaction of the four species. Responses to fragmentation differed strongly between species, but no interaction could be detected between the abundance of the different species. Thus competition within and between native and invasive species may not be regulating abundances in these regions. On the contrary, the abundance of M. ravelobensis and E. myoxinus differed significantly between study regions and was negatively affected by fragmentation. In contrast, there was no evidence of an impact of fragmentation on the abundance of M. murinus. Finally, the invasive R. rattus responded positively to the increasing distance to the continuous forest. In conclusion, the response of small Malagasy mammals to forest fragmentation varies largely between species, and fragmentation effects need to be examined at a species-specific level to fully understand their ecological dynamics and complexity.

Lemur species-specific metapopulation responses to habitat loss and fragmentation.

Determining what factors affect species occurrence is vital to the study of primate biogeography. We investigated the metapopulation dynamics of a lemur community consisting of eight species (Avahi occidentalis, Propithecus coquereli, Microcebus murinus, Microcebus ravelobensis, Lepilemur edwardsi, Cheirogaleus medius, Eulemur mongoz, and Eulemur fulvus) within fragmented tropical dry deciduous forest habitat in Ankarafantsika National Park, Madagascar. We measured fragment size and isolation of 42 fragments of forest ranging in size from 0.23 to 117.7 ha adjacent to continuous forest. Between June and November 2011, we conducted 1218 surveys and observed six of eight lemur species (M. murinus, M. ravelobensis, C. medius, E. fulvus, P. coquereli, and L. edwardsi) in the 42 fragments. We applied among patch incidence function models (IFMs) with various measures of dispersal and a mainland-island IFM to lemur species occurrence, with the aim of answering the following questions: 1) Do lemur species in dry deciduous forest fragments form metapopulations? 2) What are the separate effects of area (extinction risk) and connectivity/isolation (colonization potential) within a lemur metapopulation? 3) Within simulated metapopulations over time, how do area and connectivity/isolation affect occurrence? and 4) What are the conservation implications of our findings? We found that M. murinus formed either a mainland-island or an among patch metapopulation, M. ravelobensis formed a mainland-island metapopulation, C. medius and E. fulvus formed among patch metapopulations, and neither P. coquereli or L. edwardsi formed a metapopulation. Metapopulation dynamics and simulations suggest that area was a more consistent positive factor determining lemur species occurrence than fragment isolation and is crucial to the maintenance of lemur populations within this fragmented landscape. Using a metapopulation approach to lemur biogeography is critical for understanding how lemur species respond to forest loss and fragmentation.

The effects of a national highway on the Endangered golden-brown mouse lemurMicrocebus ravelobensisin Ankarafantsika National Park, Madagascar

AbstractAlthough roads are often assumed to be barriers to the dispersal of arboreal species, there has been little empirical testing of this assumption. If arboreal animals are unable to cross roads, population subdivision may occur, or resources may become inaccessible. We tested the hypothesis that Route Nationale 4 (RN4), a paved highway, was a barrier to movement and dispersal of the Endangered golden-brown mouse lemurMicrocebus ravelobensisin Ankarafantsika National Park, in north-west Madagascar. During June–August 2015 we conducted a capture–mark–recapture study at three sites: two adjacent to RN4 and one within intact forest without a potential barrier. During 2,294 trap nights we captured 120 golden-brown mouse lemurs 1,032 times. In roadside habitats we captured significantly more males than females, whereas the opposite was the case in interior forest habitat. We detected eighteen crossings of highway transects by nine individuals; however, all potential dispersal events involved males. In roadside habitat, movement was significantly inhibited in both males and females. We present some of the first data on the effects of roads on movement patterns in arboreal Malagasy mammals, showing species- and sex-biased effects of roads as dispersal barriers. Our findings indicate that roads may not be complete barriers to dispersal in lemurs. We recommend that conservation managers and scientists examine explicitly the effects of roads and natural arboreal bridges in Madagascar in future studies.

Variations in the excretion patterns of helminth eggs in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar.

Many factors can influence the parasite load of animal hosts, but integrative studies that simultaneously investigate several factors are still rare in many taxonomic groups. This study investigates the influence of host species, host population density, parasite transmission mode, sex, and two temporal (month, year) factors on gastrointestinal parasite prevalence and fecal egg counts of two endemic primate species from Madagascar, Microcebus ravelobensis and Microcebus murinus. A total of 646 fecal samples were available and analyzed from three dry seasons. Six different helminth egg morphotypes were found, and these were Subulura sp. (14.51 % prevalence), strongyle eggs (12.95 %), Ascaris sp. (7.94 %), Lemuricola sp. (0.17 %), and two forms of tapeworms (Hymenolepis spp.) (1.73 and 0.69 %). Coinfection with more than one egg type was observed in 21.22 % of the samples containing eggs. Multivariate analyses revealed that host species and sex did neither explain significant variation in the prevalence and fecal egg counts of parasites with direct life cycles (Ascaris sp., strongyle egg type, Lemuricola sp.) nor of arthropod-transmitted parasites (Subulura sp.). However, fecal egg counts of Subulura sp. differed significantly between study sites, and the prevalence of Subulura sp. and of parasites with direct life cycles was influenced by temporal parameters, mainly by differences between study years and partly between months. When comparing the findings with the yearly and seasonal rainfall patterns in the area, most results are in accordance with the hypothesis of an increased vulnerability of the host toward infection under some sort of environmental challenge.

Are Tropical Small Mammals Physiologically Vulnerable to Arrhenius Effects and Climate Change?

There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.

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.

The lack of female dominance in golden‐brown mouse lemurs suggests alternative routes in lemur social evolution

Female dominance is a well-known trait of lemurs, although it has not been reported from all species and is still often unexplored, especially in the nocturnal species. We examined the intersexual dominance relationships in Microcebus ravelobensis, a congener of M. murinus who is well known for its female dominance. Given the many similarities in biology, it was predicted that M. ravelobensis should also possess female dominance. Seventeen unfamiliar male-female pairs were formed with animals captured in northwestern Madagascar and kept in a two-cage setting (one cage for each animal) for up to 1 week. Four encounter experiments were conducted with each pair. In contrast to the expectations, females were not consistently dominant over their male partners. Only 3 of 17 dyads developed a clear agonistic asymmetry, among which were two cases of male dominance and only one case of female dominance. Because body mass differences did not explain the findings, various other possible explanations are discussed. It is suggested that food may not be the driving factor of female dominance in mouse lemurs. Instead, it is hypothesized that species-specific differences in the quality of sleeping sites (i.e., tree holes) and in social grouping patterns may better explain why some mouse lemur species have female dominance, whereas others like the golden-brown mouse lemur do not. It is concluded thatthese arguments and hypotheses may even hold true for other solitary foragers and may thereby lead to a better understanding of the variable social evolution in lemurs and primates in general.

Tsidy, Repahaka sy Fotsife: 15 years research on nocturnal lemurs in the Ankarafantsika National Park, Madagascar1

Tsidy, Repahaka sy Fotsife from the Malagasy: Mouse lemur, sportive lemur and woolly lemur. "The Ankarafantsika Lemur Project", is based at the field station of Ampijoroa in the National Park of Ankarafantsika in the North-West of Madagascar and is conducted by the Institute of Zoology from the University of Veterinary Medicine Hanover (Germany) in close collaboration with the local universities of Antananarivo, of Mahajanga and Madagascar National Parks (authorities for the management of protected areas in Madagascar). The project started in 1996. The goal is to enhance our knowledge on the adaptation and evolution of a previously neglected group of primates, the nocturnal lemurs, and to contribute to their conservation. Thus, researchers study the diversity, ecology, communication and socio-biology of the nocturnal lemurs. They discovered one new mouse lemur species (Microcebus ravelobensis) in this area. They characterised aspects of the morphometry, genetics, communication, ecology, social traits and recently, cognitive abilities of sympatrically living mouse-sized (Microcebus murinus and M. ravelobensis) and cat-sized lemur species (Lepilemur edwardsi and Avahi occidentalis). Some major results are presented in this article showing the importance of exchanging experience, educating Malagasy students and field guides and joint work with Malagasy partners in order to deepen our knowledge on the biology of endemic species. This knowledge is crucial to establish efficient management plans and thus contribute to the conservation of threatened species.

Experimental evidence for olfactory predator recognition in wild mouse lemurs

Although primates have remarkable olfactory capabilities, their ability for olfactory predator recognition is still understudied. We investigated this cognitive ability in wild gray and golden-brown mouse lemurs (Microcebus murinus and M. ravelobensis) that were confronted with four different olfactory stimuli, derived from two Malagasy predators (fossa and barn owl) and two local nonpredator species (brown lemur and sifaka). The predator response was tested (1) in a systematic cage setup and (2) in a two-way choice experiment with two Sherman traps on platforms in the forest (stimulus trap vs. nonstimulus trap). For part 1, the study animals were housed in cages during habituation and 5 days of experiments. One stimulus was tested per night and was presented underneath a drinking bottle. The changes in the time spent close to the stimulus and the drinking time at the bottle were used as indicators of predator recognition. A timidity score was established by classifying the strength of the antipredator response during the experiment. The study animals spent significantly less time drinking and less time in the stimulus area when confronted with fossa odor compared with the other stimuli. The timidity score was significantly higher during the fossa stimulus compared with the nonpredator and the control stimuli. The two-way choice experiments revealed a complete avoidance of the fossa odor, which was not found with the other stimuli. Thus, wild mouse lemurs showed clear signs of olfactory predator recognition in the case of the fossa in both experiments, but no signs of avoidance to the other presented stimuli. The lack of owl avoidance may be explained by less or no aversive metabolites in the owl stimulus or by lower significance for olfactory recognition of aerial predators. Furthermore, the results showed slight differences between the two mouse lemur species that may be linked to differences in their ecology.

Different competitive potential in two coexisting mouse lemur species in northwestern Madagascar

Interspecific competition has been suggested to influence the biogeographic distribution patterns of species. A high competitive potential could entail species-specific advantages during resource acquisition that could translate into a higher potential for range expansion. We investigated whether differences in the competitive potential of the morphologically similar and partially sympatric gray mouse lemur (Microcebus murinus) and golden-brown mouse lemur (Microcebus ravelobensis) may help to explain differences in their geographic range sizes. We carried out encounter experiments with 14 pairs of captured female mouse lemurs of both species. The experimental dyads were tested in a two-cage arrangement, with individuals being separated from each other outside the experiments. Two days of habituation and four subsequent days of 1-h encounter experiments were conducted, before releasing the animals again in the wild. In general, the M. murinus individuals won significantly more conflicts than their partners. In eight of 14 tested pairs, there was a significant species bias in winning conflicts, and in 87.5% of these dyads, M. murinus was the "dyad winner". A high competitive potential did not depend on body mass. Furthermore, "dyad winners" spent more time feeding (P < 0.05) and were less spatially restricted than "dyad losers". To conclude, our results suggest that the widely distributed M. murinus may indeed have a higher competitive potential than the regional endemic M. ravelobensis, which may, among other possible factors, have enabled this species to expand geographically, despite the presence of other competing congeners.