A habitat stronghold on the precipice: A call-to-action for supporting lemur conservation in northeast Madagascar.

The northeast of Madagascar is as diverse as it is threatened. The area bordering the Analanjirofo and SAVA regions contains six protected areas and at least 22 lemur species. Many applied research and conservation programs have been established in the region with the aim of ensuring both wildlife and people thrive in the long term. While most of the remaining humid evergreen forest of northeast Madagascar is formally protected, the local human population depends heavily on the land, and unsustainable natural resource use threatens this biodiversity hotspot. Drawing from our collective experiences managing conservation activities and research programs in northeast Madagascar, we discuss the major threats to the region and advocate for eight conservation activities that help reduce threats and protect the environment, providing specific examples from our own programs. These include (1) empowering local conservation actors, (2) ensuring effectively protected habitat, (3) expanding reforestation, (4) establishing and continuing long-term research and monitoring, (5) reducing food insecurity, (6) supporting environmental education, (7) promoting sustainable livelihoods, and (8) expanding community health initiatives. Lastly, we provide a list of actions that individuals can take to join us in supporting and promoting lemur conservation.

Predicting primate-parasite associations using exponential random graph models.

Ecological associations between hosts and parasites are influenced by host exposure and susceptibility to parasites, and by parasite traits, such as transmission mode. Advances in network analysis allow us to answer questions about the causes and consequences of traits in ecological networks in ways that could not be addressed in the past. We used a network-based framework (exponential random graph models or ERGMs) to investigate the biogeographic, phylogenetic and ecological characteristics of hosts and parasites that affect the probability of interactions among nonhuman primates and their parasites. Parasites included arthropods, bacteria, fungi, protozoa, viruses and helminths. We investigated existing hypotheses, along with new predictors and an expanded host-parasite database that included 213 primate nodes, 763 parasite nodes and 2319 edges among them. Analyses also investigated phylogenetic relatedness, sampling effort and spatial overlap among hosts. In addition to supporting some previous findings, our ERGM approach demonstrated that more threatened hosts had fewer parasites, and notably, that this effect was independent of hosts also having a smaller geographic range. Despite having fewer parasites, threatened host species shared more parasites with other hosts, consistent with loss of specialist parasites and threat arising from generalist parasites that can be maintained in other, non-threatened hosts. Viruses, protozoa and helminths had broader host ranges than bacteria, or fungi, and parasites that infect non-primates had a higher probability of infecting more primate species. The value of the ERGM approach for investigating the processes structing host-parasite networks provided a more complete view on the biogeographic, phylogenetic and ecological traits that influence parasite species richness and parasite sharing among hosts. The results supported some previous analyses and revealed new associations that warrant future research, thus revealing how hosts and parasites interact to form ecological networks.

Population viability and harvest sustainability for Madagascar lemurs.

Subsistence hunting presents a conservation challenge by which biodiversity preservation must be balanced with safeguarding of human livelihoods. Globally, subsistence hunting threatens primate populations, including Madagascar's endemic lemurs. We used population viability analysis to assess the sustainability of lemur hunting in Makira Natural Park, Madagascar. We identified trends in seasonal hunting of 11 Makira lemur species from household interview data, estimated local lemur densities in populations adjacent to focal villages via transect surveys, and quantified extinction vulnerability for these populations based on species-specific demographic parameters and empirically derived hunting rates. We compared stage-based Lefkovitch with periodic Leslie matrices to evaluate the impact of regional dispersal on persistence trajectories and explored the consequences of perturbations to the timing of peak hunting relative to the lemur birth pulse, under assumptions of density-dependent reproductive compensation. Lemur hunting peaked during the fruit-abundant wet season (March-June). Estimated local lemur densities were roughly inverse to body size across our study area. Life-history modeling indicated that hunting most severely threatened the species with the largest bodies (i.e., Hapalemur occidentalis, Avahi laniger, Daubentonia madagascariensis, and Indri indi), characterized by late-age reproductive onsets and long interbirth intervals. In model simulations, lemur dispersal within a regional metapopulation buffered extinction threats when a majority of local sites supported growth rates above the replacement level but drove regional extirpations when most local sites were overharvested. Hunt simulations were most detrimental when timed to overlap lemur births (a reality for D. madagascariensis and I. indri). In sum, Makira lemurs were overharvested. Regional extirpations, which may contribute to broad-scale extinctions, will be likely if current hunting rates persist. Cessation of anthropogenic lemur harvest is a conservation priority, and development programs are needed to help communities switch from wildlife consumption to domestic protein alternatives.

The changing ecology of primate parasites: Insights from wild-captive comparisons.

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity-a rarely studied yet widespread human-driven host movement-can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro- (helminths and arthropods) and micro-parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally-including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector-borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non-close contact, including through fecal-oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

Phylogeny and Divergence Times of Lemurs Inferred with Recent and Ancient Fossils in the Tree.

Paleontological and neontological systematics seek to answer evolutionary questions with different data sets. Phylogenies inferred for combined extant and extinct taxa provide novel insights into the evolutionary history of life. Primates have an extensive, diverse fossil record and molecular data for living and extinct taxa are rapidly becoming available. We used two models to infer the phylogeny and divergence times for living and fossil primates, the tip-dating (TD) and fossilized birth-death process (FBD). We collected new morphological data, especially on the living and extinct endemic lemurs of Madagascar. We combined the morphological data with published DNA sequences to infer near-complete (88% of lemurs) time-calibrated phylogenies. The results suggest that primates originated around the Cretaceous-Tertiary boundary, slightly earlier than indicated by the fossil record and later than previously inferred from molecular data alone. We infer novel relationships among extinct lemurs, and strong support for relationships that were previously unresolved. Dates inferred with TD were significantly older than those inferred with FBD, most likely related to an assumption of a uniform branching process in the TD compared with a birth-death process assumed in the FBD. This is the first study to combine morphological and DNA sequence data from extinct and extant primates to infer evolutionary relationships and divergence times, and our results shed new light on the tempo of lemur evolution and the efficacy of combined phylogenetic analyses.

Interactions between plants and primates shape community diversity in a rainforest in Madagascar.

Models of ecological community assembly predict how communities of interacting organisms may be shaped by abiotic and biotic factors. Competition and environmental filtering are the predominant factors hypothesized to explain community assembly. This study tested the effects of habitat, phylogenetic and phenotypic trait predictors on species co-occurrence patterns and abundances, with the endemic primates of Madagascar as an empirical system. The abundance of 11 primate species was estimated along gradients of elevation, food resource abundance and anthropogenic habitat disturbance at local scales in south-east Madagascar. Community composition was compared to null models to test for phylogenetic and functional structure, and the effects of phylogenetic relatedness of co-occurring species, their trait similarity and environmental variables on species' abundances were tested using mixed models and quantile regressions. Resource abundance was the strongest predictor of community structure. Where food tree abundance was high, closely related species with similar traits dominated communities. High-elevation communities with lower food tree abundance consisted of species that were distantly related and had divergent traits. Closely related species had dissimilar abundances where they co-occurred, partially driven by trait dissimilarity, indicating character displacement. By integrating local-scale variation in primate community composition, evolutionary relatedness and functional diversity, this study found strong evidence that community assembly in this system can be explained by competition and character displacement along ecological gradients.

Compounding impacts of COVID-19, cyclone and price crash on vanilla farmers' food security and natural resource use.

The intersection of the COVID-19 pandemic with other crises can amplify vulnerabilities and push communities further into poverty. In low-income countries, the dual impacts of COVID-19 and extreme weather events, along with multidimensional poverty and structural vulnerabilities in agriculture can decimate farmer livelihoods. This study aims to understand the effects of individual and compounding crises (COVID-19, cyclones, and vanilla price collapse) on smallholder vanilla farmers and local coping strategies in Madagascar, one of the world's largest vanilla producers and poorest countries. We used semi-structured and scenario-based interviews across two case study villages with contrasting enforcement of forest regulations. We found that the impact of the pandemic, combined with the cyclone event, disrupted livelihoods, resulting in income losses and food security challenges that exacerbated farmer vulnerabilities. Sixty eight percent of households reported crop losses due to strong winds and heavy rainfall brought by cyclone Enawo in 2017. The COVID-19 outbreak struck the region just as the residents were recovering from the effects of the cyclone. COVID-19-related travel restrictions in the aftermath of the cyclone took a substantial economic toll, with 54.1% of respondents experiencing a decline in earnings, and 17% facing a total loss of income due to the imposed lockdown. The decline in vanilla prices at the onset of 2020 had a far-reaching additional impact, affecting not only farmers but also residents who rely on other sources of income. Local communities reported using the forest resources more frequently as a safety net during crises in the village with more lenient regulations. This study underscores the importance of understanding the interconnectedness and compounding impacts of cascading crises on food security and natural resource use. We highlight the need for a comprehensive approach to increasing farmer resilience, particularly for those reliant on global market crops such as vanilla.

Astroviruses in terrestrial Malagasy mammals.

Small terrestrial mammals are major hosts of infectious agents responsible for zoonotic diseases. Astroviruses (AstVs)-the cause of non-bacterial gastroenteritis mainly affecting young children-have been detected in a wide array of mammalian and avian host species. However, understanding the factors that influence AstV infection within and across hosts is limited. Here, we investigated the impact of land use changes on AstVs in terrestrial small mammals in rural northeastern Madagascar. We sampled 515 small mammals, representing seven endemic and four introduced species. Twenty-two positive samples were identified, all but one of which were found in the introduced species Mus musculus and Rattus rattus (family Muridae), with a positivity rate of 7.7% (6/78) and 5.6% (15/266), respectively. The non-introduced rodent case was from an endemic shrew-tenrec (family Tenrecidae). We found the highest positivity rate of AstVs infection in brushy regrowth (17.5%, 7/40) as compared to flooded rice fields (4.60%, 8/174), secondary forest (4.1%, 3/74), agroforest (3.6%, 1/28), village (2.61%, 3/115), and semi-intact forest (0%, 0/84). A phylogenetic analysis revealed an association between AstVs and their rodent host species. None of the viruses were phylogenetically related to AstVs previously described in Malagasy bats. This study supports AstV circulation in synanthropic animals in agricultural habitats of Madagascar and highlights the need to assess the spillover risk to human populations in rural areas.

Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data.

We tested four major hypotheses on the ecological aspects of body mass variation in extant Malagasy strepsirrhines: thermoregulation, resource seasonality/scarcity, resource quality, and primary productivity. These biogeographic hypotheses focus on the ecological aspects of body mass variation, largely ignoring the role of phylogeny for explaining body mass variation within lineages. We tested the independent effects of climate and resource-related variables on variation in body mass among Malagasy primates using recently developed comparative methods that account for phylogenetic history and spatial autocorrelation. We extracted data on lemur body mass and climate variables for a total of 43 species from 39 sites. Climatic data were obtained from the WorldClim database, which is based on climate data from weather stations compiled around the world. Using generalized linear models that incorporate parameters to account for phylogenetic and spatial autocorrelation, we found that diet and climate variables were weak predictors of lemur body mass. Moreover, there was a strong phylogenetic effect relative to the effects of space on lemur body mass in all models. Thus, we failed to find support for any of the four hypotheses on patterns of geography and body mass in extant strepsirrhines. Our results indicate that body mass has been conserved since early in the evolutionary history of each genus, while species diversified into different environmental niches. Our findings are in contrast to some previous studies that have suggested resource and climate related effects on body mass, though these studies have examined this question at different taxonomic and/or geographic scales.

Morphological variation of Rattus rattus Linnaeus, 1758 (Rodentia: Muridae) in forest and anthropogenic habitats of a watershed in northeastern Madagascar.

De par sa haute capacité d'adaptation et la plasticité de son alimentation, reflétée par une variation morphologique des individus, Rattus rattus s'est dispersé et a occupé un large éventail d'habitats à Madagascar après son introduction qui date du Xe siècle environ. Cette étude s'intéresse à la variation morphologique de cette espèce superposée à différents modes d'utilisation du paysage. Nous avons analysé des données morphométriques crânio-dentaires recueillies à partir de 333 spécimens capturés dans le bassin-versant de la rivière Manantenina sur la partie orientale du Massif de Marojejy. Les résultats des tests MANOVA comparant la morphologie crânio-dentaire et la taille des individus par sexe, classe d'âge et type d'habitat ont montré qu'il existe des différences significatives entre la forme du crâne et la taille des individus parmi les types d'habitat et la classe d'âge. Aucun dimorphisme sexuel n'a été trouvé sur la morphologie du crâne, par contre la taille des mâles est significativement plus grande par rapport à celle des femelles. Les individus vivant en dehors de l'habitat forestier ont des crânes nettement plus gros (Tukey HSD, p = 0,004). Comme anticipé, les jeunes individus ont un crâne plus petit que les adultes et les adultes plus âgés, mais la largeur de leur première molaire, la longueur de la rangée de dents de la mandibule et la longueur de la couronne de la rangée de molaire maxillaire sont plus grandes. Due to their high adaptability and dietary plasticity, reflected by individual morphological variation, Rattus rattus has dispersed to and occupies a broad range of habitats on Madagascar after its introduction to the island, which dates towards the 10th century. This study focuses on morphological variation of this species overlaid on different human land use patterns.We analyzed cranio-dental morphometric data collected from 333 specimens captured in the Manantenina River valley on the eastern side of the Marojejy Massif.The results of the MANOVA tests comparing cranio-dental morphology and size of individuals by sex, age class, and habitat type showed that there are significant differences between skull shape and size of individuals among the habitat types and age classes. No sexual dimorphism based on cranio-dental morphology was found but we noted a significant difference between male and female body size between different habitats. Individuals living outside of native forest have distinctly larger skulls (Tukey HSD, p = 0,004). As anticipated, young individuals have a smaller skull than adults and old adults, however the breadth of their first molar, length of mandible toothrow, and crown length of maxillary molar row are proportionally larger.

Comparing transmission potential networks based on social network surveys, close contacts and environmental overlap in rural Madagascar.

Social and spatial network analysis is an important approach for investigating infectious disease transmission, especially for pathogens transmitted directly between individuals or via environmental reservoirs. Given the diversity of ways to construct networks, however, it remains unclear how well networks constructed from different data types effectively capture transmission potential. We used empirical networks from a population in rural Madagascar to compare social network survey and spatial data-based networks of the same individuals. Close contact and environmental pathogen transmission pathways were modelled with the spatial data. We found that naming social partners during the surveys predicted higher close-contact rates and the proportion of environmental overlap on the spatial data-based networks. The spatial networks captured many strong and weak connections that were missed using social network surveys alone. Across networks, we found weak correlations among centrality measures (a proxy for superspreading potential). We conclude that social network surveys provide important scaffolding for understanding disease transmission pathways but miss contact-specific heterogeneities revealed by spatial data. Our analyses also highlight that the superspreading potential of individuals may vary across transmission modes. We provide detailed methods to construct networks for close-contact transmission pathogens when not all individuals simultaneously wear GPS trackers.

Predictions of primate-parasite coextinction.

Future biodiversity loss threatens the integrity of complex ecological associations, including among hosts and parasites. Almost half of primate species are threatened with extinction, and the loss of threatened hosts could negatively impact parasite associations and ecosystem functions. If endangered hosts are highly connected in host-parasite networks, then future host extinctions will also drive parasite extinctions, destabilizing ecological networks. If threatened hosts are not highly connected, however, then network structure should not be greatly affected by the loss of threatened hosts. Networks with high connectance, modularity, nestedness and robustness are more resilient to perturbations such as the loss of interactions than sparse, nonmodular and non-nested networks. We analysed the interaction network involving 213 primates and 763 parasites and removed threatened primates (114 species) to simulate the effects of extinction. Our analyses revealed that connections to 23% of primate parasites (176 species) may be lost if threatened primates go extinct. In addition, measures of network structure were affected, but in varying ways because threatened hosts have fewer parasite interactions than non-threatened hosts. These results reveal that host extinctions will perturb the host-parasite network and potentially lead to secondary extinctions of parasites. The ecological consequences of these extinctions remain unclear. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Food insecurity related to agricultural practices and household characteristics in rural communities of northeast Madagascar.

Ending hunger and alleviating poverty are key goals for a sustainable future. Food security is a constant challenge for agrarian communities in low-income countries, especially in Madagascar. We investigated agricultural practices, household characteristics, and food security in northeast Madagascar. We tested whether agricultural practices, demographics, and socioeconomics in rural populations were related to food security. Over 70% of respondents reported times during the last three years during which food for the household was insufficient, and the most frequently reported cause was small land size (57%). The probability of food insecurity decreased with increasing vanilla yield, rice yield, and land size. There was an interaction effect between land size and household size; larger families with smaller land holdings had higher food insecurity, while larger families with larger land had lower food insecurity. Other socioeconomic and agricultural variables were not significantly related to food insecurity, including material wealth, education, crop diversity, and livestock ownership. Our results highlight the high levels of food insecurity in these communities and point to interventions that would alleviate food stress. In particular, because current crop and livestock diversity were low, agricultural diversification could improve outputs and mitigate food insecurity. Development of sustainable agricultural intensification, including improving rice and vanilla cultivation to raise yields on small land areas, would likely have positive impacts on food security and alleviating poverty. Increasing market access and off-farm income, as well as improving policies related to land tenure could also play valuable roles in mitigating challenges in food security. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12571-021-01179-3.

Effects of land use, habitat characteristics, and small mammal community composition on Leptospira prevalence in northeast Madagascar.

Human activities can increase or decrease risks of acquiring a zoonotic disease, notably by affecting the composition and abundance of hosts. This study investigated the links between land use and infectious disease risk in northeast Madagascar, where human subsistence activities and population growth are encroaching on native habitats and the associated biota. We collected new data on pathogenic Leptospira, which are bacteria maintained in small mammal reservoirs. Transmission can occur through close contact, but most frequently through indirect contact with water contaminated by the urine of infected hosts. The probability of infection and prevalence was compared across a gradient of natural moist evergreen forest, nearby forest fragments, flooded rice and other types of agricultural fields, and in homes in a rural village. Using these data, we tested specific hypotheses for how land use alters ecological communities and influences disease transmission. The relative abundance and proportion of exotic species was highest in the anthropogenic habitats, while the relative abundance of native species was highest in the forested habitats. Prevalence of Leptospira was significantly higher in introduced compared to endemic species. Lastly, the probability of infection with Leptospira was highest in introduced small mammal species, and lower in forest fragments compared to other habitat types. Our results highlight how human land use affects the small mammal community composition and in turn disease dynamics. Introduced species likely transmit Leptospira to native species where they co-occur, and may displace the Leptospira species naturally occurring in Madagascar. The frequent spatial overlap of people and introduced species likely also has consequences for public health.

Primate diversification inferred from phylogenies and fossils.

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ∼600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ∼34 Ma, but also elevated extinction ∼10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.

Testing the adaptive radiation hypothesis for the lemurs of Madagascar.

Lemurs, the diverse, endemic primates of Madagascar, are thought to represent a classic example of adaptive radiation. Based on the most complete phylogeny of living and extinct lemurs yet assembled, I tested predictions of adaptive radiation theory by estimating rates of speciation, extinction and adaptive phenotypic evolution. As predicted, lemur speciation rate exceeded that of their sister clade by nearly twofold, indicating the diversification dynamics of lemurs and mainland relatives may have been decoupled. Lemur diversification rates did not decline over time, however, as predicted by adaptive radiation theory. Optimal body masses diverged among dietary and activity pattern niches as lineages diversified into unique multidimensional ecospace. Based on these results, lemurs only partially fulfil the predictions of adaptive radiation theory, with phenotypic evolution corresponding to an 'early burst' of adaptive differentiation. The results must be interpreted with caution, however, because over the long evolutionary history of lemurs (approx. 50 million years), the 'early burst' signal of adaptive radiation may have been eroded by extinction.