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Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar's biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus Microcebus, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework., Competing Interests: Competing interests: The authors declare no competing interests., (© 2024. The Author(s).)

We present the first open-access, island-wide isotopic database (IsoMad) for modern biologically relevant materials collected on Madagascar within the past 150 years from both terrestrial and nearshore marine environments. Isotopic research on the island has increasingly helped with biological studies of endemic organisms, including evaluating foraging niches and investigating factors that affect the spatial distribution and abundance of species. The IsoMad database should facilitate future work by making it easy for researchers to access existing data (even for those who are relatively unfamiliar with the literature) and identify both research gaps and opportunities for using various isotope systems to answer research questions. We also hope that this database will encourage full data reporting in future publications., (© 2024. The Author(s).)

Objectives: The investigation of morphological variation in animals is widely used in taxonomy, ecology, and evolution. Using large datasets for meta-analyses has dramatically increased, raising concerns about dataset compatibilities and biases introduced by contributions of multiple researchers., Materials and Methods: We compiled morphological data on 13 variables for 3073 individual mouse lemurs (Cheirogaleidae, Microcebus spp.) from 25 taxa and 153 different sampling locations, measured by 48 different researchers. We introduced and applied a filtering pipeline and quantified improvements in data quality (Shapiro-Francia statistic, skewness, and excess kurtosis). The filtered dataset was then used to test for genus-wide sexual size dimorphism and the applicability of Rensch's, Allen's, and Bergmann's rules., Results: Our pipeline reduced inter-observer bias (i.e., increased normality of data distributions). Inter-observer reliability of measurements was notably variable, highlighting the need to reduce data collection biases. Although subtle, we found a consistent pattern of sexual size dimorphism across Microcebus, with females being the larger (but not heavier) sex. Sexual size dimorphism was isometric, providing no support for Rensch's rule. Variations in tail length but not in ear size were consistent with the predictions of Allen's rule. Body mass and length followed a pattern contrary to predictions of Bergmann's rule., Discussion: We highlighted the usefulness of large multi-researcher datasets for testing ecological hypotheses after correcting for inter-observer biases. Using genus-wide tests, we outlined generalizable patterns of morphological variability across all mouse lemurs. This new methodological toolkit aims to facilitate future large-scale morphological comparisons for a wide range of taxa and applications., (© 2023 Wiley Periodicals LLC.)

Adenoviruses (AdVs) are important human and animal pathogens and are frequently used as vectors for gene therapy and vaccine delivery. Surprisingly, there are only scant data regarding primate AdV origin and evolution, especially in the most basal primate hosts. We detect and sequence AdVs from faeces of two Madagascan lemur species. Complete genome sequence analyses define a new AdV species with a particularly large gene encoding a protein of unknown function in the early gene region 3. Unexpectedly, the new AdV species is not most similar to human or other simian AdVs but to bat adenovirus C. Genome characterisation shows signals of virus-host codivergence in non-structural genes, which show lower diversity than structural genes. Outside a lemur species mixing zone, recombination less frequently separates structural genes, as in human adenovirus C. The evolutionary history of lemur AdVs likely involves both a host switch and codivergence with the lemur hosts., Competing Interests: None declared., (© The Author(s) 2023. Published by Oxford University Press.)

Background: Fleshy fruits evolved to be attractive to seed dispersers through various signals such as color and scent. Signals can evolve through different trajectories and have various degrees of reliability. The strongest substrate on which reliable signals can evolve is when there is an inherent link between signal and reward, rendering cheating costly or impossible. It was recently proposed that aliphatic esters in fruit scent may be predictive of sugar content due to their synthesis from products of sugar fermentation. We test this hypothesis on a case study of wild fig species (Ficus tiliifolia) from Madagascar, which relies on seed dispersal by lemurs., Results: We found a strong positive correlation between signal (esters) and reward (sugar). We also found that non-esters, including direct fermentation products, in fruit scent do not indicate sugar levels, which implies that this relationship is not simply a product of fruit maturation wherein more mature fruits emit more scent and contain more sugar., Conclusions: While based on a single taxon, these results strongly support the hypothesis that a biochemical link between ester synthesis and sugar may render the ester fraction of fruit scent an honest signal for fruit quality, with consequences for animal sensory and feeding ecology, and the evolution of plants in the context of seed dispersal., (© 2022. The Author(s).)

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Microsatellites have been a workhorse of evolutionary genetic studies for decades and are still commonly in use for estimating signatures of genetic diversity at the population and species level across a multitude of taxa. Yet, the very high mutation rate of these loci is a double-edged sword, conferring great sensitivity at shallow levels of analysis (e.g. paternity analysis) but yielding considerable uncertainty for deeper evolutionary comparisons. For the present study, we used reduced representation genome-wide data (restriction site-associated DNA sequencing (RADseq)) to test for patterns of interspecific hybridization previously characterized using microsatellite data in a contact zone between two closely related mouse lemur species in Madagascar ( Microcebus murinus and Microcebus griseorufus ). We revisit this system by examining populations in, near, and far from the contact zone, including many of the same individuals that had previously been identified as hybrids with microsatellite data. Surprisingly, we find no evidence for admixed nuclear ancestry. Instead, re-analyses of microsatellite data and simulations suggest that previously inferred hybrids were false positives and that the program NewHybrids can be particularly sensitive to erroneously inferring hybrid ancestry. Combined with results from coalescent-based analyses and evidence for local syntopic co-occurrence, we conclude that the two mouse lemur species are in fact completely reproductively isolated, thus providing a new understanding of the evolutionary rate whereby reproductive isolation can be achieved in a primate.

Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases., (© 2022. The Author(s).)

The role of plant secondary metabolites (PSMs) in shaping the feeding decisions, habitat suitability, and reproductive success of herbivorous mammals has been a major theme in ecology for decades. Although primatologists were among the first to test these ideas, studies of PSMs in the feeding ecology of non-human primates have lagged in recent years, leading to a recent call for primatologists to reconnect with phytochemists to advance our understanding of the primate nutrition. To further this case, we present a formal meta-analysis of diet choice in response to PSMs based on field studies on wild primates. Our analysis of 155 measurements of primate feeding response to PSMs is drawn from 53 studies across 43 primate species which focussed primarily on the effect of three classes of PSMs tannins, phenolics, and alkaloids. We found a small but significant effect of PSMs on the diet choice of wild primates, which was largely driven by the finding that colobine primates showed a moderate aversion to condensed tannins. Conversely, there was no evidence that PSMs had a significant deterrent effect on food choices of non-colobine primates when all were combined into a single group. Furthermore, within the colobine primates, no other PSMs influenced feeding choices and we found no evidence that foregut anatomy significantly affected food choice with respect to PSMs. We suggest that methodological improvements related to experimental approaches and the adoption of new techniques including metabolomics are needed to advance our understanding of primate diet choice., (© 2022 The Authors. American Journal of Primatology published by Wiley Periodicals LLC.)

Increasing anthropogenic disturbances in Madagascar are exerting constrains on endemic Malagasy lemurs and their habitats, with possible effects on their health and survival. An important component of health is the gut microbiome, which might be disrupted by various stressors associated with environmental change. We have studied the gut microbiome of gray-brown mouse lemurs ( Microcebus griseorufus ), one of the smallest Malagasy primates and an important model of the convergent evolution of diseases. We sampled two sites: one situated in a national park and the other consisting of a more disturbed site around human settlement. We found that more intense anthropogenic disturbances indeed disrupted the gut microbiome of this lemur species marked by a reduction in bacterial diversity and a shift in microbial community composition. Interestingly, we noted a decrease in beneficial bacteria (i.e., members of the Bacteroidaceae family) together with a slight increase in disease-associated bacteria (i.e., members of the Veillonellaceae family), and alterations in microbial metabolic functions. Because of the crucial services provided by the microbiome to pathogen resistance and host health, such negative alterations in the gut microbiome of mouse lemurs inhabiting anthropogenically disturbed habitats might render them susceptible to diseases and ultimately affecting their survival in the shrinking biodiversity seen in Madagascar. Gut microbiome analyses might thus serve as an early warning signal for pending threats to lemur populations., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Wasimuddin, Malik, Ratovonamana, Rakotondranary, Ganzhorn and Sommer.)

Until recently, the study of major histocompability complex (MHC) mediated immunity has focused on the direct link between MHC diversity and susceptibility to parasite infection. However, MHC genes can also influence host health indirectly through the sculpting of the bacterial community that in turn shape immune responses. We investigated the links between MHC class I and II gene diversity gut microbiome diversity and micro- (adenovirus, AdV) and macro- (helminth) parasite infection probabilities in a wild population of non-human primates, mouse lemurs of Madagascar. This setup encompasses a plethora of underlying interactions between parasites, microbes and adaptive immunity in natural populations. Both MHC classes explained shifts in microbiome composition and the effect was driven by a few select microbial taxa. Among them were three taxa (Odoribacter, Campylobacter and Prevotellaceae-UCG-001) which were in turn linked to AdV and helminth infection status, correlative evidence of the indirect effect of the MHC via the microbiome. Our study provides support for the coupled role of MHC diversity and microbial flora as contributing factors of parasite infection., Competing Interests: The authors have declared that no competing interests exist.

Diel activity patterns of animal species reflect constraints imposed by morphological, physiological, and behavioral trade-offs, but these trade-offs are rarely quantified for multispecies assemblages. Based on a systematic year-long camera-trap study in the species-rich mammal assemblage of Lake Manyara National Park (Tanzania), we estimated activity levels (hours active per day) and circadian rhythms of 17 herbivore and 11 faunivore species to determine the effects of body mass and trophic level on activity levels and cathemerality (the degree to which species are active throughout the day and night). Using generalized least squares and phylogenetic generalized least squares analyses, we found no support for the hypothesis that trophic level is positively associated with activity levels. We found no support for activity levels to scale positively with body mass in herbivores or to differ between ruminants and nonruminants; in faunivores, we also did not detect relationships between body mass and activity levels. Cathemerality was positively associated with activity levels but did not scale significantly with body mass. Overall, our findings caution against trophic level or body mass-associated generalized conclusions with regard to diel activity patterns., Competing Interests: None declared., (© 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Forest restoration is a prime goal within the 2021-2030 UN "Decade of Ecosystem Resoration". As part of these activities, natural regeneration has to be promoted for biological as well as for economic reasons. For this, the processes of seed dispersal, seed predation and germination have to be understood in the original as well as in degraded vegetation formations. We used seed removal experiments to assess post-dispersal processes that influence recruitment along a gradient of forest degradation in Madagascar analyzing seeds of three animal dispersed tree species. The percentage of seeds consumed or dispersed, declined from forest (28.6%) to degraded forest (17.2%) to savanna (10.8%). Only three out of 1080 seeds were cached and remained intact during the 14-day experiment. All three seeds were cached in the forest habitat and none in the degraded forest and savanna. The low percentage of seeds removed may be due to the lack of endemic rodents caching seeds, as only introduced rats were recorded in the area. The species-poor fauna of potential secondary seed dispersers of the region and especially in the degraded areas might represent an obstacle for diverse regeneration in degraded regions of Madagascar., (© 2021. The Author(s).)

Thorough knowledge of the ecology of a species or population is an essential prerequisite for understanding the impact of ecology on the evolution of their respective social systems. Because of their diversity of social organizations, baboons ( Papio spp.) are a useful model for comparative studies. Comparative ecological information was missing for Guinea baboons ( Papio papio ), however. Here we provide data on the ecology of Guinea baboons in a comparative analysis on two geographical scales. First, we compare climate variables and land cover among areas of occurrence of all six baboon species. Second, we describe home range size, habitat use, ranging behaviour, and diet from a local population of Guinea baboons ranging near the Centre de Recherche de Primatologie (CRP) Simenti in the Niokolo-Koba National Park, Senegal. Home ranges and daily travel distances at Simenti varied seasonally, yet the seasonal patterns in their daily travel distance did not follow a simple dry vs. rainy season pattern. Chemical food composition falls within the range of other baboon species. Compared to other baboon species, areas occupied by Guinea baboons experience the highest variation in precipitation and the highest seasonality in precipitation. Although the Guinea baboons' multi-level social organization is superficially similar to that of hamadryas baboons ( P. hamadryas ), the ecologies of the two species differ markedly. Most Guinea baboon populations, including the one at Simenti, live in more productive habitats than hamadryas baboons. This difference in the ecology of the two species contradicts a simple evolutionary relation between ecology and social system and suggests that other factors have played an additional role here., Competing Interests: The authors declare that they have no conflict of interest., (Copyright: © 2021 Dietmar Zinner et al.)

Traditional socio-ecological models consider that folivorous primates experience limited feeding competition due to the low quality, high abundance, and even distribution of leaves. Evidence from several folivorous species that experience similar constraints to frugivores does not support this hypothesis. The sympatric lemur genera Avahi (Indriidae) and Lepilemur (Lepilemuridae) are good models to understand how food availability constrains folivores since they are both nocturnal, folivorous, and have a comparable body mass. Here we investigate how two nocturnal folivorous primates, Avahi meridionalis and Lepilemur fleuretae, living in the lowland rain forest of Tsitongambarika, South-East Madagascar, partition their dietary niche and are influenced by seasonality of young leaves. To account for food availability, we collected annual phenological data on 769 trees from 200 species. We also collected behavioural data on 5 individuals per lemur species from August 2015 to July 2016 via continuous focal sampling. We found the phenological profile to be seasonal with peaks of leaf flushing, flowering, and fruiting occurring in the austral summer. The two species showed limited dietary overlap (37% rich period, 6% lean period), and A. meridionalis showed higher feeding time and longer daily distances travelled during the rich period. Lepilemur fleuretae showed a dietary shift during the lean period, relying more on mature leaves (73.3% during the lean period, 13.5% during the rich period) but maintaining similar activity levels between seasons. The time spent feeding on food items by A. meridionalis was positively correlated with the nitrogen content and negatively correlated with polyphenols during the rich period. We highlighted a clear effect of the seasonality of young leaves on the diet, nutritional content, activity patterns, and daily distances travelled by two folivorous species, which can be linked to nutrient balancing and time-minimising versus energy-maximising strategies., (© 2021 S. Karger AG, Basel.)

Little is known about the presence of vector-borne bacteria in southwest Madagascar. Anthropogenic alteration of natural habitats represents an important driver for the emergence of new diseases. Especially the involvement of livestock and the involuntary maintaining of invasive synanthropic animals (particularly rats) facilitate disease transmission from wildlife to humans and associated animals and vice versa. The dissemination or acquisition of ectoparasites is most likely in regions where human/wildlife contact is increasing. Little is known about the presence of vector-borne bacteria in southwest Madagascar. In 2016 and 2017, ectoparasites were collected from various introduced (cattle and goats, cats, dogs and chicken, rats and mice) and native animal species (mouse lemurs [Microcebus griseorufus], Grandidier's mongooses [Galidictis grandidieri], bastard big-footed mice [Macrotarsomys bastardi], greater hedgehog tenrecs [Setifer setosus] and lesser hedgehog tenrecs [Echinops telfairi]) in the northern portion of Tsimanampetsotsa National Park and the adjacent littoral region. Thirteen species of blood-feeding ectoparasites (235 individuals of ticks [5 species], 414 lice [4 spp.] and 389 fleas [4 spp.]) were investigated for the presence and identity of rickettsiae, borreliae, bartonellae and Yersinia pestis using PCR techniques. Rickettsia spp. were detected in every single ectoparasite species (Amblyomma variegatum, A. chabaudi, Rhipicephalus microplus, Haemaphysalis simplex, Argas echinops, Ctenocephalides felis, Echidnophaga gallinacea, Pulex irritans, Xenopsylla cheopis, Haematopinus quadripertusus, Linognathus africanus, L. vituli, Lemurpediculus verruculosus). Lice and ticks were found harboring rickettsiae identified as Rickettsia africae, while Rickettsia felis-like bacteria were associated with fleas. Borrelia spp. were detected in 5% of H. simplex and 1% of R. microplus ticks. Bartonella spp. were detected in 40% of H. quadripertusus pools and in 5% of L. verruculosus pools. Y. pestis was detected in X. cheopis and E. gallinacea fleas collected from a rat. This study presents the detection of a broad spectrum of vector-borne bacteria including potential pathogens, and an unexpected finding of Y. pestis far off the known plague foci in Madagascar., Competing Interests: Declaration of Competing Interest None., (Copyright © 2020 The Authors. Published by Elsevier B.V. All rights reserved.)

Adenovirus (AdV) infections are one of the main causes of diarrhea in young children. Enteric AdVs probably disrupt gut microbial defences, which can result in diarrhea. To understand the role of the gut microbiome in AdV-induced pathologies, we investigated the gut microbiome of a naturally AdV-infected non-human primate species, the Malagasy mouse lemur (Microcebus griseorufus), which represents an important model in understanding the evolution of diseases. We observed that AdV infection is associated with disruption of the gut microbial community composition. In AdV+ lemurs, several commensal taxa essential for a healthy gut microbiome decreased, whereas genera containing potential pathogens, such as Neisseria, increased in abundance. Microbial co-occurrence networks revealed a loss of important microbial community interactions in AdV+ lemurs and an overrepresentation of Prevotellaceae. The observation of enteric virus-associated loss of commensal bacteria and associated shifts towards pathobionts may represent the missing link for a better understanding of AdV-induced effects in humans, and also for their potential as drivers of co-infections, an area of research that has been largely neglected so far.

Plant species with fleshy fruits offer animals rewards such as sugar, protein, and fat, to feed on their fruits and disperse their seeds. They have also evolved visual and olfactory signals indicating their presence and ripeness.In some systems, fruit color serves as a reliable visual signal of nutrient content. Yet even though many volatile chemicals used as olfactory signals derive from nutrients animals seek, it is still unknown whether fruit scent encodes information regarding nutrient content in wild fruits.We examine the relationship between olfactory signals and nutrient rewards in 28 fruiting plant species in Madagascar. We measured the relative amounts of four chemical classes in fruit scent using gas chromatography and mass spectrometry, as well as the relative amounts of sugar and protein in fruit pulp.We found that protein levels are not associated with elevated amounts of chemically related volatile compounds in fruit scent. In contrast, sugar content is strongly associated with the chemical composition of fruit scent.To our knowledge, this is the first research to explore the connection between fruit chemical signals and nutrient rewards. Our results imply that in the case of sugar, fruit scent is predictive of nutrient content and hence an honest signal., Competing Interests: The authors have no competing interests., (© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Human encroachment of natural habitats bears the threat of disease transmission between native and introduced species that had not come into contact before, thus promoting the spread of new diseases in both directions. This is a matter of concern especially in areas where human-wildlife contact has not been intense in the recent past. In southwest Madagascar, we collected ectoparasites from various mammalian hosts and chicken, and examined their host preferences and their prevalence in relation to season and habitat degradation. Field-work took place in the northern portion of Tsimanampetsotsa National Park and the adjacent coastal strip (littoral) in the dry and in the rainy season of 2016/2017. Endemic mammals were trapped with live traps placed in habitats of different degrees of degradation: 1) relatively pristine forest, 2) degraded forest, 3) cultivated and shrub land. Rats and mice were also trapped in 4) villages. We identified 17 species of ectoparasites (296 individuals of ticks [5 species], 535 lice [7 spp.], 389 fleas [4 spp.] and 13 mites [1 sp.]) collected from 15 host species. There was no indication for seasonal or habitat effects on parasite infection. A large portion of the parasites was host-specific. Some ectoparasite species were shared either by several endemic or by several introduced species, but apart from the introduced flea species Echidnophaga gallinacea (collected from six different hosts including the endemic carnivore Galidictis grandidieri) no other ectoparasite species was shared between endemic and introduced host species., (Copyright © 2019 Elsevier B.V. All rights reserved.)

Objectives: Geophagy has several hypothesized functions, among them (1) detoxification of plant secondary compounds, for example, tannins, (2) buffering stomach pH to alleviate acidosis caused by high sugar intake, and (3) supplementing the diet with mineral nutrients. We tested these hypotheses in Nepal gray langurs (Semnopithecus schistaceus), a foregut fermenter for which fruits and leaves dominate the diet at different times of the year., Materials and Methods: We collected data on feeding time per food item for 21 unprovisioned adult langurs at Ramnagar, Nepal, for 1 year using instantaneous sampling (773 observation hours). We combined these data with relative sugar and tannin content of food items to estimate diet content. We collected rainfall data to distinguish the wet season (May-September) from the dry season (October-April). We collected soil samples from consumption and control sites to test for pH and sodium, potassium, magnesium, and calcium concentrations., Results: Langurs consumed soil from two sources: termite structures (in almost all months) and river banks and beds (mainly in the dry season). Soil feeding was not positively correlated with dietary tannin or sugar content (GLMM). Soil pH was not high enough to buffer stomach contents. Only sodium was significantly higher in consumed soil., Discussion: The most likely function of geophagy was the acquisition of sodium. This conclusion is consistent with reports for other animals. Buffering stomach pH, an often-suggested function for animals with ruminant-like digestion, was not supported. Detoxification, often proposed for animals with a diet high in secondary compounds, was also not supported., (© 2018 Wiley Periodicals, Inc.)

Long-term genetic monitoring of populations is essential for efforts aimed at preserving genetic diversity of endangered species. Here, we employ a framework of long-term genetic monitoring to evaluate the effects of fragmentation and the effectiveness of the establishment of corridors in restoring population connectivity and genetic diversity of mouse lemurs Microcebus ganzhorni . To this end, we supplement estimates of neutral genetic diversity with the assessment of adaptive genetic variability of the major histocompatibility complex (MHC). In addition, we address the challenges of long-term genetic monitoring of functional diversity by comparing the genotyping performance and estimates of MHC variability generated by single-stranded conformation polymorphism (SSCP)/Sanger sequencing with those obtained by high-throughput sequencing (next-generation sequencing [NGS], Illumina), an issue that is particularly relevant when previous work serves as a baseline for planning management strategies that aim to ensure the viability of a population. We report that SSCP greatly underestimates individual diversity and that discrepancies in estimates of MHC diversity attributable to the comparisons of traditional and NGS genotyping techniques can influence the conclusions drawn from conservation management scenarios. Evidence of migration among fragments in Mandena suggests that mouse lemurs are robust to the process of fragmentation and that the effect of corridors is masked by ongoing gene flow. Nonetheless, results based on a larger number of shared private alleles at neutral loci between fragment pairs found after the establishment of corridors in Mandena suggest that gene flow is augmented as a result of enhanced connectivity. Our data point out that despite low effective population size, M. ganzhorni maintains high individual heterozygosity at neutral loci and at MHC II DRB gene and that selection plays a predominant role in maintaining MHC diversity. These findings highlight the importance of long-term genetic monitoring in order to disentangle between the processes of drift and selection maintaining adaptive genetic diversity in small populations.

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Fluctuations in food availability are a major challenge faced by primates living in seasonal climates. Variation in food availability can be especially challenging for females, because of the high energetic costs of reproduction. Therefore, females must adapt the particular demands of the different reproductive stages to the seasonal availability of resources. Madagascar has a highly seasonal climate, where food availability can be extremely variable. We investigated the seasonal changes in diet composition, nutrient and energy intake of female and male sifakas (Propithecus verreauxi) in a dry deciduous forest in western Madagascar. We examined how females adjust their diet to different reproductive stages. Seasonality affected the diet of both sexes; particularly in the dry season (Apr-Oct) with low availability of food items, especially fruits, males and females had a reduced nutrient and energy intake compared to the wet season (Nov-Mar) with higher food and fruit availability. The comparison of the diet between sexes in different reproductive stages showed that during the late stage of lactation (Nov-Jan) females had higher food intake, and as a result they had a higher intake of macronutrients (crude protein, fat and non-structured carbohydrates (TNC)) and energy than males. These differences were not present during the pregnancy of females, with both sexes having similar intake of macronutrients and energy during that stage. The increase in the intake of macronutrients observed for females during late lactation could be related to the higher energetic demands of this stage of reproduction. Thus, the observed pattern in the diet indicates that sifaka females are following a capital breeding strategy, whereby females potentially store enough nutrients to cope with the reproduction costs in periods of low food availability., (© 2016 Wiley Periodicals, Inc.)

Protein limitation has been considered a key factor in hypotheses on the evolution of life history and animal communities, suggesting that animals should prioritize protein in their food choice. This contrasts with the limited support that food selection studies have provided for such a priority in nonhuman primates, particularly for folivores. Here, we suggest that this discrepancy can be resolved if folivores only need to select for high protein leaves when average protein concentration in the habitat is low. To test the prediction, we applied meta-analyses to analyze published and unpublished results of food selection for protein and fiber concentrations from 24 studies (some with multiple species) of folivorous primates. To counter potential methodological flaws, we differentiated between methods analyzing total nitrogen and soluble protein concentrations. We used a meta-analysis to test for the effect of protein on food selection by primates and found a significant effect of soluble protein concentrations, but a non-significant effect for total nitrogen. Furthermore, selection for soluble protein was reinforced in forests where protein was less available. Selection for low fiber content was significant but unrelated to the fiber concentrations in representative leaf samples of a given forest. There was no relationship (either negative or positive) between the concentration of protein and fiber in the food or in representative samples of leaves. Overall our study suggests that protein selection is influenced by the protein availability in the environment, explaining the sometimes contradictory results in previous studies on protein selection. Am. J. Primatol. 79:e22550, 2017. © 2016 Wiley Periodicals, Inc., (© 2016 Wiley Periodicals, Inc.)

The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.

Objectives: The proximate and ultimate determinants that may have prompted some primates to shift from an arboreal to terrestrial feeding niche, whether due to environmental change, seasonality, and/or predation pressure, are poorly understood. Within a fragmented littoral forest in southeast Madagascar, an arboreal strepsirrhine population spends a large proportion of time on the ground, thus we aimed to identify which factors influence terrestrial feeding., Methods: From January to December 2013, we conducted 103 full-day focal follows on three social groups of southern bamboo lemurs H. meridionalis. We continuously recorded feeding time on all arboreal and terrestrial items, as well as whether the focal individual was under the canopy or exposed, and the distance to their nearest conspecific neighbor. All observed food items were collected and analyzed for macronutrient content. Daily climatic variables (temperature, precipitation), resource seasonality, daily path length (DPL), along with dietary and predation risk proxies, were used as fixed effects in a linear mixed model, with the daily proportion of terrestrial feeding as the dependent variable., Results: Our model indicated that daily terrestrial feeding increased at cooler temperature, was associated with reduced DPL, and the intake of dietary metabolizable energy increased as terrestrial feeding increased. All other fixed effects were not significant predictors., Discussion: Our study provides a window into the ultimate determinants of niche expansion: ancestral primates, in absence of their primary resources, may have initially descended to the ground in peripheral population range areas where the benefits (e g., nutritional pay-off) out-weighed the costs., (© 2016 Wiley Periodicals, Inc.)

Phylogeographic analysis can be described as the study of the geological and climatological processes that have produced contemporary geographic distributions of populations and species. Here, we attempt to understand how the dynamic process of landscape change on Madagascar has shaped the distribution of a targeted clade of mouse lemurs (genus Microcebus) and, conversely, how phylogenetic and population genetic patterns in these small primates can reciprocally advance our understanding of Madagascar's prehuman environment. The degree to which human activity has impacted the natural plant communities of Madagascar is of critical and enduring interest. Today, the eastern rainforests are separated from the dry deciduous forests of the west by a large expanse of presumed anthropogenic grassland savanna, dominated by the Family Poaceae, that blankets most of the Central Highlands. Although there is firm consensus that anthropogenic activities have transformed the original vegetation through agricultural and pastoral practices, the degree to which closed-canopy forest extended from the east to the west remains debated. Phylogenetic and population genetic patterns in a five-species clade of mouse lemurs suggest that longitudinal dispersal across the island was readily achieved throughout the Pleistocene, apparently ending at ∼55 ka. By examining patterns of both inter- and intraspecific genetic diversity in mouse lemur species found in the eastern, western, and Central Highland zones, we conclude that the natural environment of the Central Highlands would have been mosaic, consisting of a matrix of wooded savanna that formed a transitional zone between the extremes of humid eastern and dry western forest types.

Objectives: Small-bodied folivores are rare because processing leaves often requires extensive gut adaptations and lengthy retention times for fiber fermentation. However, the <1 kg nocturnal white-footed sportive lemurs (Lepilemur leucopus) persist on a leaf-based diet. We investigated how extrinsic (i.e., seasonality in temperature and food availability) and intrinsic factors (i.e., reproductive state) influence nutrient intake and explored how nutrient and energy needs are met in this species., Materials and Methods: We conducted full night focal follows across all seasons and analyzed nutrients in all items eaten by adults of both sexes to investigate nutrient intake and nutritional priorities in L. leucopus. We estimated digestible protein content, as this is a biologically more meaningful measure than crude protein., Results: Protein intake was constant across seasons, while non-protein energy and dry matter intake increased from the hot wet to the cold dry season. Males and females did not differ in their nutrient or apparent energy intake irrespective of female reproductive state., Discussion: We conclude that these animals prioritize protein over non-protein energy intake as dietary protein is in limited supply, and that thermoregulation poses higher energetic costs than reproduction in this species. While protein intake did not differ across female reproductive states, the relative protein content of the diet was highest during the lactation period, indicating that the balance of non-protein to protein intake may be more important than absolute intake. Dry matter intake was high compared to other folivorous primates, indicating that L. leucopus follows an intake rather than an efficiency strategy to meet its energy requirements. Am J Phys Anthropol 160:197-207, 2016. © 2016 Wiley Periodicals, Inc., (© 2016 Wiley Periodicals, Inc.)

Selection of sleeping sites has consequences for individual fitness. Non-human primates often bias their selection towards arboreal sites, and the lemurs of Madagascar typically rest/sleep in trees, tree holes, and/or constructed nests. Three non-mutually exclusive hypotheses to explain sleeping site selection include protection from predators, avoidance of parasitic vectors, and improved thermoregulation. Here, we examine these hypotheses for the unusual sleeping site selections by the southern bamboo lemur (Hapalemur meridionalis). Within the Mandena littoral forest of southeast Madagascar, the southern bamboo lemur is known for its ecological flexibility compared to other bamboo lemur species, including a dietary niche expansion to feeding on the ground. Between October 2012 and December 2013, we observed bamboo lemurs from three social groups for 1778.67 h, conducting full-day focal follows on 11 adult individuals (five males, six females). During this period, all three groups were observed to sleep on the ground, with one of these groups also using an abandoned nest of a Madagascar crested ibis (Lophotibis cristata). We collected habitat and temperature data to examine whether selection was influenced by environmental variables. Terrestrial sleeping (N = 17) was observed in all individuals but one adult female, with individuals burrowing under thick vegetation more often during the hot austral summer. While difficult to rigorously test, it is possible that terrestrial sleep sites and/or sleeping in a bird nest may impair visual detection by some aerial and terrestrial predators. Neither of these sites (i.e., terrestrial sleeping or use of a bird nest), however, is likely to minimize exposure to parasites/vectors. Terrestrial sleeping appears to support a thermoregulatory strategy, whereas the use of a bird nest could not be empirically tested. Our observations of unique sleeping site locations used by southern bamboo lemurs further the complexity of their natural history and that of Malagasy strepsirrhines.

Dietary characteristics and environmental variables are important selective factors directing ecological diversification in rodents. On Madagascar, the introductions and spread of the commensal black rat (Rattus rattus) can be seen as example cases to study dietary niche occupation and dietary adaptation in an insular environment. We investigate how tooth wear as a measure of dietary adaptation of black rats differs between four distinct habitats (village, manioc fields, spiny forest, and rainforest) with different dietary resources. We use the 3D surface texture analysis (3DST, using 30 parameters according to ISO 25178) as a measure of dietary abrasiveness. 3DST is applied on the occlusal surface of the upper first molar of 37 black rat specimens. The rainforest sample displays less rough and less voluminous surface textures compared to the village samples as indicated by smaller values for height parameters (Sa, Sp, Sq), inverse areal material ratio (Smc), and volume parameters (Vm, Vmc, Vmp, Vv, and Vvc). We therefore rank sampling areas from highest to lowest abrasiveness (village>manioc fields/spiny forest>rainforest). The rats from villages and rainforest differ to such an extent that one could have interpreted them to belong to different species. This indicates a high degree of variability in terms of ingesta abrasiveness. Furthermore, the pronounced difference between rats from human habitations compared to rats from associated fields or natural vegetation is interpreted to clearly indicate shifts in dietary niche occupation in relation to human impact.

Little is known about the role of endemic ticks as vectors for bacterial and protozoan pathogens for animals and humans in Madagascar and their interaction in anthropogenic habitats where humans, their livestock and native Malagasy species (vectors and hosts) come into more frequent contact than in natural forest ecosystems. The aims of the study were (1) to test whether habitat degradation is associated with increased infestation of tortoises by ticks and (2) to investigate whether ticks carried Babesia, Borrelia or Rickettsia species that might be pathogenic for humans and livestock. We studied hard ticks of two endemic Malagasy tortoises, Astrochelys radiata and Pyxis arachnoides in March and April 2013 in southwest Madagascar. Two tortoise habitats were compared, the National Park of Tsimanampetsotsa and the adjacent degraded pasture and agricultural land at the end of the wet season. Ticks were screened for protozoan and bacterial pathogens via PCR on DNA isolated from ticks using genus-specific primers. Only one out of 42 A. radiata collected from both habitats had ticks. The low prevalence did not allow further analyses of the effect of habitat degradation. Forty-two P. arachnoides were found in the anthropogenic habitat and 36 individuals in the national park. Tick infestation rates of P. arachnoides differed significantly between the two study sites. Tortoises inside the park had lower tick prevalence than outside (8 of 36 (22%) versus 32 of 42 individuals (76%)) and infected animals tended to have fewer ticks inside than outside the park. All ticks collected in both habitats were adults of the ixodid tick Amblyomma chabaudi, which is supposed to be a host-specific tick of P. arachnoides. Screening for Borrelia sp. and Babesia sp. was negative in all ticks. But all A. chabaudi ticks were infected with Rickettsia africae, known to cause spotted fever in humans. Thus, habitat degradation seems to be linked to higher infestation of tortoises with ticks with possible consequences for humans and their livestock., (Copyright © 2015 Elsevier GmbH. All rights reserved.)

Austronesians colonized the islands of Rapa Nui, Hawaii, the Marquesas and Madagascar. All of these islands have been found to harbor Austronesian artifacts and also, all of them are known nesting sites for marine turtles. Turtles are well known for their transoceanic migrations, sometimes totalling thousands of miles, between feeding and nesting grounds. All marine turtles require land for nesting. Ancient Austronesians are known to have had outstanding navigation skills, which they used to adjust course directions. But these skills will have been insufficient to locate tiny, remote islands in the vast Indo-Pacific oceans. We postulate that the Austronesians must have had an understanding of the marine turtles' migration patterns and used this knowledge to locate remote and unknown islands. The depth and speed at which marine turtles migrate makes following them by outrigger canoes feasible. Humans have long capitalized on knowledge of animal behavior., (Copyright © 2015 Académie des sciences. Published by Elsevier SAS. All rights reserved.)

The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations.

Most frugivorous bats are efficient seed dispersers, as they typically do not damage seeds and transport them over long distances. In contrast, bats of the phyllostomid genus Chiroderma cheat fig trees by acting more as seed predators than as seed dispersers. The bats initially separate seeds from fruit pulp in the mouth. After extracting the juice from the fruit pulp, they thoroughly chew the seeds and spit out small seed fragments in a pellet. Consequently, the faeces contain almost no viable seeds. We compared the nutrient content of intact fig seeds with ejecta and faecal samples from both Chiroderma villosum and the 'conventional' frugivorous bat Artibeus watsoni. We show that C. villosum can extract nutrients from the seeds, especially protein and fat. The processing time of figs showed no significant difference between the two bat species. Food-choice experiments showed that C. villosum preferred fig species with more seeds over those with fewer seeds. This preference, in combination with the specialized seed-chewing behaviour, leads to an increased nutrient intake per fig. This unique strategy enables C. villosum to satisfy its nutritional requirements with a lower number of figs than other species, which decreases the amount of energy necessary for foraging flights as well as the predation risk during foraging., (© 2015. Published by The Company of Biologists Ltd.)

Biodiversity continues to decline in the face of increasing anthropogenic pressures such as habitat destruction, exploitation, pollution and introduction of alien species. Existing global databases of species' threat status or population time series are dominated by charismatic species. The collation of datasets with broad taxonomic and biogeographic extents, and that support computation of a range of biodiversity indicators, is necessary to enable better understanding of historical declines and to project - and avert - future declines. We describe and assess a new database of more than 1.6 million samples from 78 countries representing over 28,000 species, collated from existing spatial comparisons of local-scale biodiversity exposed to different intensities and types of anthropogenic pressures, from terrestrial sites around the world. The database contains measurements taken in 208 (of 814) ecoregions, 13 (of 14) biomes, 25 (of 35) biodiversity hotspots and 16 (of 17) megadiverse countries. The database contains more than 1% of the total number of all species described, and more than 1% of the described species within many taxonomic groups - including flowering plants, gymnosperms, birds, mammals, reptiles, amphibians, beetles, lepidopterans and hymenopterans. The dataset, which is still being added to, is therefore already considerably larger and more representative than those used by previous quantitative models of biodiversity trends and responses. The database is being assembled as part of the PREDICTS project (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems - http://www.predicts.org.uk). We make site-level summary data available alongside this article. The full database will be publicly available in 2015.

Understanding the drivers of species adaptations to changing environments on the one hand and the limits for hybridization on the other hand is among the hottest questions in evolutionary biology. Parasites represent one of the major selective forces driving host evolution and at least those with free-living stages are at the same time dependent on the ecological conditions of their host's habitat. Local immunological adaptations of host species to varying parasite pressure are therefore expected and might represent the genetic basis for ecological speciation and the maintenance of recently diverged species. Madagascar provides one of the rare examples where two partially sympatric primate species (Microcebus griseorufus, M. murinus) and their hybrids, as well as an allopatric species (M. cf rufus) live in close proximity along a very steep environmental gradient ranging from southern dry spiny bush to gallery forest to evergreen eastern humid rain forest, thus mimicking the situation encountered during extensions and retreats of vegetation formations under changing climatic conditions. This system was used to study parasite infection and immune gene (MHC) adaptations to varying parasite pressure that might provide selective advantages to pure species over hybrids. Parasite burdens increased with increasing humidity. M. griseorufus, M. murinus, and their hybrids but not M. rufus shared the same MHC alleles, indicating either retention of ancestral polymorphism or recent gene flow. The hybrids had much higher prevalence of intestinal parasites than either of the parent species living under identical environmental conditions. The different representation of parasites can indicate a handicap for hybrids that maintains species identities.

We address the question why papers dealing with the ecology of primates are so sparsely represented in the general ecological literature. A literature analyses based on entries in Web of Science and PrimateLit reveals that despite a large number of papers published on primates in general and on the ecology of primates, only a very small fraction of these papers is published in high-ranking international ecological journals. We discuss a number of potential reasons for the disproportion and highlight the problems associated with experimental research on wild primates and constraints on sample size as major issues.

Ecologists want to explain why populations of animals are not evenly distributed across landscapes and often turn to nutritional explanations. In seeking to link population attributes with food quality, they often contrast nutritionally positive traits, such as the concentration of nitrogen, against negative ones, such as fibre concentration, by using a ratio of these traits. This specific ratio has attracted attention because it sometimes correlates with the biomass of colobine primates across sites in Asia and Africa. Although empirically successful, we have identified problems with the ratio that may explain why it fails under some conditions to predict colobine biomass. First, available nitrogen, rather than total nitrogen, is nutritionally important, while the presence of tannins is the major factor reducing the availability of nitrogen in browse plant species. Second, tannin complexes inflate measures of fibre. Finally, simple ratios may be unsound statistically because they implicitly assume isometric relationships between variables. We used data on the chemical composition of plants from three continents to examine the relationships between the concentrations of nitrogen, available nitrogen, fibre and tannins in foliage and to evaluate the nitrogen to fibre ratio. Our results suggest that the ratio of the concentration of nitrogen to fibre in leaves does sometimes closely correlate with the concentration of available nitrogen. However, the ratio may give misleading results when leaves contain high concentrations of tannins. The concentration of available nitrogen, which incorporates measures of total nitrogen, dry matter digestibility and tannins, should give a better indication of the nutritional value of leaves for herbivorous mammals that can readily be extrapolated to habitats.

Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson's rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these "rules" and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses (δ(15)N and δ(13)C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ(13)C values, indicating that M. griseorufus feeds more on C(4) and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ(15)N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.

Flexibility in physiological processes is essential to adequately respond to changes in environmental conditions. Madagascar is a particularly challenging environment because climatic conditions seem less predictable than in comparative ecosystems in other parts of the world. We used the reddish-gray mouse lemur (Microcebus griseorufus) from the most unpredictable environment in Madagascar as a model to investigate the flexibility of energy saving strategies to cope with the unpredictability of their habitat. For this we measured T (sk) of free-ranging mouse lemurs throughout the year using temperature data loggers. M. griseorufus showed a very strong seasonal as well as an individual flexibility in thermoregulation. During the rainy season all M. griseorufus remained normothermic. At the beginning of the dry season individuals started to exhibit different energy saving strategies: irregular short torpor bouts, regular daily torpor, prolonged torpor of a few days, and hibernation over several weeks. The accumulation of sufficient seasonal body fat was the crucial factor determining the thermal behavior of individuals. The observed intraspecific and sex independent variation in thermoregulatory patterns within one population inhabiting the same small geographical area is exceptional and gives M. griseorufus the ability to respond to current environmental as well as individual conditions. This thermal plasticity might be seen as a key to success and survival for M. griseorufus in an extremely unpredictable environment.