Intraspecific agonism plays a role in accessing key resources for survival and reproduction, such as food and mates, in many nonhuman primates. Female dominance and fission-fusion dynamics (i.e., fluctuating subgroup size and composition) are two adaptive strategies used by some primate species to cope with a high degree of seasonality. We investigated how seasonal fluctuations in reproductive opportunities and food availability affect group-wide agonism rates in wild black-and-white ruffed lemurs (Varecia variegata), a species with high fission-fusion dynamics and female dominance that exhibits strict seasonal and communal breeding but does not consistently breed annually. We conducted focal animal sampling over four years, encompassing several mating and birth seasons for V. variegata across two sites. We summed all agonistic interactions within the focal animal’s subgroup to calculate biweekly agonism rates. We estimated fruit and flower abundance using semimonthly phenological surveys. We found a significant effect of reproductive season on agonism, such that agonism rates were highest during the mating season (vs. nonreproductive and birth seasons), particularly in years when mating and births were observed. Subgroup size was also a major driver of agonism, with higher rates of agonism in larger subgroups, although subgroup size did not significantly affect individual rates of agonism. Fruit and flower availabilities were not significant predictors of agonism, suggesting that agonistic interactions in V. variegata may be mitigated by other means such as fission-fusion dynamics. Overall, these findings suggest that agonism functions as a reproductive strategy in V. variegata, and potentially in other female-dominant or communally breeding primate species, as a mechanism for females to exert mate choice and for males to gain access to mating opportunities.
Tree species preference is an understudied yet crucial component of sustainable forest management, as unsustainable harvesting can lead to non-random loss of functional traits. We examine wood resource preference across five regions of Madagascar's biodiverse eastern humid forests. We asked forest users in 19 men's and 19 women's focus groups to list their preferred tree species for common short- (charcoal, firewood) and long-term (house construction, furniture, tools) uses. We then measured functional traits of 260 preferred and common tree species: height, DBH, bark thickness, specific leaf area, wood specific gravity, and seed dispersal syndrome in the surrounding landscape. Using household interviews, we determined the average distance households would need to travel to access each species. Forest users preferred shorter travel distances for short-term uses, whereas species preferences for long-term uses were associated with specific functional traits. Women focused mainly on firewood and tool provisioning and were more likely to prefer species at a shorter walking distance than men. We found no clear relationships between tree species preference and dispersal syndromes, suggesting that a diverse community of seed-dispersing animal species may be necessary to maintain traits preferred for tree harvest in Malagasy humid forests. We suggest strategies to support reducing deforestation, promoting traditional ecological knowledge, and increasing accessibility of wood resources to women.
Despite extensive conservation efforts worldwide, biodiversity loss continues, particularly in tropical regions. It is, therefore, essential to develop biodiversity monitoring methods that can be effectively scaled up in both time and space, enabling wildlife managers to quickly assess and respond to changes in populations or communities. We explored the effectiveness of combining camera traps with acoustic methods to survey seed dispersing birds and mammals. We deployed arboreal and terrestrial camera traps alongside AudioMoth sound recorders with varying recording schedules to survey 220 sampling locations across five distinct sites in Madagascar’s eastern humid forests, though acoustic analyses were limited to one site. Based on all three methods (arboreal, terrestrial camera trap and AudioMoths), we successfully identified 78
Studies can only guide conservation if their findings are informative at the scales at which practitioners and policy-makers operate. Yet, it is rarely tested whether large-scale studies reach similar conclusions to the smaller-scale studies on which conservation traditionally relies. We examine whether predictors of extinction risk are consistent across global, regional, and local scales, for 210 tropical forest mammal species (≥1 kg) that existed during the last 130,000 years, in 64 tropical forests, across three biogeographical realms. We found consistent predictors of extinction risk (body mass, generation length, diet, brain volume, and scansoriality) when analyses differed only in their spatial resolution. However, predictors differed when analyses also varied in their temporal extent. Macroecological findings about extinction risk can, thus, inform conservation at smaller scales, but they risk misidentifying threatened species if differences in temporal extent are not recognized.
Tropical forests hold most of Earth's biodiversity and a higher concentration of threatened mammals than other biomes. As a result, some mammal species persist almost exclusively in protected areas, often within extensively transformed and heavily populated landscapes. Other species depend on remaining remote forested areas with sparse human populations. However, it remains unclear how mammalian communities in tropical forests respond to anthropogenic pressures in the broader landscape in which they are embedded. As governments commit to increasing the extent of global protected areas to prevent further biodiversity loss, identifying the landscape-level conditions supporting wildlife has become essential. Here, we assessed the relationship between mammal communities and anthropogenic threats in the broader landscape. We simultaneously modeled species richness and community occupancy as complementary metrics of community structure, using a state-of-the-art community model parameterized with a standardized pan-tropical data set of 239 mammal species from 37 forests across 3 continents. Forest loss and fragmentation within a 50-km buffer were associated with reduced occupancy in monitored communities, while species richness was unaffected by them. In contrast, landscape-scale human density was associated with reduced mammal richness but not occupancy, suggesting that sensitive species have been extirpated, while remaining taxa are relatively unaffected. Taken together, these results provide evidence of extinction filtering within tropical forests triggered by anthropogenic pressure occurring in the broader landscape. Therefore, existing and new reserves may not achieve the desired biodiversity outcomes without concurrent investment in addressing landscape-scale threats.
How plants respond to weather seasonality is a fundamental evolutionary question that is particularly relevant to understand as climate change alters weather patterns across the globe. Although temperature and light conditions primarily cue flowering in temperate plants, the weather cues that tropical plants use to regulate their phenological cycles are lesser known. We studied the weather‐related ultimate causes of flowering and fruiting patterns in six woody perennial species found in the evergreen lowland humid forests of southeastern Madagascar by investigating the associations between biweekly weather (i.e. rainfall, temperature and insolation) and species‐level flowering and fruiting phenology. We then developed process‐based models to identify the potential proximate weather cues that these species use to regulate their flowering time. Given the region's strong rainfall seasonality, we hypothesised that the reproductive timing of these species would mainly be constrained by water availability. These species flowered asynchronously, at different times of the year and after a variety of weather conditions, including drought, cool temperatures, warm temperatures and low light. The flowering and fruiting patterns of only two species suggested that water stress constrained their phenology in support of the water limitation and optimal time of germination hypotheses. The flowering patterns of these six species did not align with the insolation limitation hypothesis, providing no evidence to suggest that light stress constrained their phenology. Cool temperature was most likely a proximate flowering cue for only one of these perennial tropical species, which contrasts with the ubiquitous influence that low temperatures have on temperate flowering phenology. Light limitation most likely influenced the flowering time of two species, paralleling the photoperiod flowering cues that some temperate plants use. The timescales at which these potential flowering cues operated were species‐specific, spanning 1–7 months. Synthesis . The diverse associations we identified between weather and flowering patterns suggest that the phenology of these perennial tropical plants evolved in response to different selective pressures and will likely have variable responses to climate change.
Forest loss and degradation due to land cover changes imperil biodiversity worldwide. Subtropical and tropical ecosystems experience high deforestation rates, negatively affecting species like primates. Madagascar's endemic lemurs face exceptionally high risks of population declines and extirpation. We examined how short-term land cover changes within a fragmented landscape in southeastern Madagascar impacted the density of lemur species. Using line transects, we assessed density changes in nine lemur species across five forest fragments. Diurnal surveys were conducted monthly from 2015 to 2019 on 35 transects (total effort = 1268 km). Additionally, 21 transects were surveyed nocturnally in 2015 and 2016 (total effort = 107.5 km). To quantify forest cover changes, we generated land use/land cover (LULC) maps from Sentinel-2 imagery using supervised classification for each year. For the LULC maps, we overlayed species-specific buffers around all transects and calculated the proportion of land cover classes within them. We observed declines in the annual densities of four diurnal and cathemeral lemur species between 2015 and 2019, with species-specific declines of up to 80% (Varecia variegata). While the density of two nocturnal species decreased, one increased fivefold (Cheirogaleus major) between 2015 and 2016. By 2019, Grassland was the dominant land type (50%), while Paddy Fields had the smallest coverage (1.03%). Mature Agricultural Land increased the most (63.37%), while New Agricultural Land decreased the most (-66.36%). Unexpectedly, we did not find evidence that higher forest cover supported a higher lemur population density within sampled areas, but we found support for the negative impact of degraded land cover types on three lemur species. Our study underscores the urgent need to address land-use changes and their repercussions for primate populations in tropical ecosystems. The diverse responses of lemur species to modified habitats highlight the complexity of these impacts and emphasize the importance of targeted conservation efforts.
Madagascar has a harsh and stochastic climate because of regular natural disturbances. This history of regular cyclones has been hypothesised to have directed evolutionary changes to lemur behaviour and morphology that make them more resilient to sudden environmental change. These adaptations may include: small group sizes, high degrees of energy-conserving behaviours, generalist habitat use, small home ranges, small body size, and a limited number of frugivorous species. To date, however, no one has tested how variation in cyclone exposure across Madagascar is associated with variation in these resilience traits. In this study, we created a detailed cyclone impact map for Madagascar using Koppen-Geiger climate class, historical cyclone tracks, the Saffir Class of cyclone and hurricane intensity, and precipitation data. We also used existing literature to calculate a resilience score for 26 lemur species for which data existed on resilience traits. Our cyclone impact map was then overlaid on known geographic ranges of these species and compared to resilience score while controlling for phylogenetic non-independence and spatial autocorrelation. We found no association between cyclone impact in a lemur range and their resilience score. When assessing traits individually, however, we found that cyclone impact was positively associated with body size, suggesting that the more impacted a species is by cyclones the smaller they are. We also found cyclone impact to be negatively associated with frugivory, with species in higher impact zones eating more fruit. While unexpected, this could reflect an increased production in fruit in tree fall gaps following cyclones. While we did not find a pattern between cyclone impact and behavioural resilience in lemurs, we suggest a similar study at a global scale across all primates would allow for more taxonomic variation and reveal larger patterns key to understanding past and future vulnerability to natural disturbances in primates.
Changes in lunar illumination alter the balance of risks and opportunities for animals, influencing activity patterns and species interactions. We examined if and how terrestrial mammals respond to the lunar cycle in some of the darkest places: the floors of tropical forests. We analysed long-term camera trapping data on 86 mammal species from 17 protected forests on three continents. Conservative categorization of activity during the night revealed pronounced avoidance of moonlight (lunar phobia) in 12 species, compared with pronounced attraction to moonlight (lunar philia) in only three species. However, half of all species in our study responded to lunar phases, either changing how nocturnal they were, altering their overall level of activity, or both. Avoidance of full moon was more common, exhibited by 30% of all species compared with 20% of species that exhibited attraction. Nocturnal species, especially rodents, were over-represented among species that avoided full moon. Artiodactyla were more prominent among species attracted to full moon. Our findings indicate that lunar phases influence animal behaviour even beneath the forest canopy. Such impacts may be exacerbated in degraded and fragmented forests. Our study offers a baseline representing relatively intact and well-protected contexts together with an intuitive approach for detecting activity shifts in response to environmental change.
Aim Tropical regions harbour over half of the world's mammals and birds, but how their communities have assembled over evolutionary timescales remains unclear. To compare eco-evolutionary assembly processes between tropical mammals and birds, we tested how hypotheses concerning niche conservatism, environmental stability, environmental heterogeneity and time-for-speciation relate to tropical vertebrate community phylogenetic and functional structure. Location Tropical rainforests worldwide. Time periodPresent. Major taxa studied Ground-dwelling and ground-visiting mammals and birds. Methods We used in situ observations of species identified from systematic camera trap sampling as realized communities from 15 protected tropical rainforests in four tropical regions worldwide. We quantified standardized phylogenetic and functional structure for each community and estimated the multi-trait phylogenetic signal (PS) in ecological strategies for the four regional species pools of mammals and birds. Using linear regression models, we test three non-mutually exclusive hypotheses by comparing the relative importance of colonization time, palaeo-environmental changes in temperature and land cover since 3.3 Mya, contemporary seasonality in temperature and productivity and environmental heterogeneity for predicting community phylogenetic and functional structure. Results Phylogenetic and functional structure showed non-significant yet varying tendencies towards clustering or dispersion in all communities. Mammals had stronger multi-trait PS in ecological strategies than birds (mean PS: mammal = 0.62, bird = 0.43). Distinct dominant processes were identified for mammal and bird communities. For mammals, colonization time and elevation range significantly predicted phylogenetic clustering and functional dispersion tendencies respectively. For birds, elevation range and contemporary temperature seasonality significantly predicted phylogenetic and functional clustering tendencies, respectively, while habitat diversity significantly predicted functional dispersion tendencies. Main conclusions Our results reveal different eco-evolutionary assembly processes structuring contemporary tropical mammal and bird communities over evolutionary timescales that have shaped tropical diversity. Our study identified marked differences among taxonomic groups in the relative importance of historical colonization and sensitivity to environmental change.
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.
Forest fragmentation may lead to substantial declines in food availability for primary consumers, especially presenting a challenge for frugivores, such as the Critically Endangered black-and-white ruffed lemur (Varecia variegata). We investigated how forest fragmentation impacts the diet and activity budgets of V. variegata across three forest fragments—71 ha, 232 ha, and 597 ha—in Kianjavato, Madagascar. We collected phenological and lemur behavioural data over 17 months. We found that in both small fragments (< 500 ha), there was lower tree basal area, tree species diversity, and availability of fruit from large tree species compared to the largest fragment. Despite overall lower fruit availability, we found that individuals in the smallest forest maintained a high degree of frugivory year-round but had high measures of dietary diversity. In contrast, individuals in the other small-fragment consumed large proportions of flowers seasonally and showed low dietary diversity. These individuals consumed nectar from the traveller’s tree (Ravenala sp.) for more than 40
Primates, represented by 521 species, are distributed across 91 countries primarily in the Neotropic, Afrotropic, and Indo-Malayan realms. Primates inhabit a wide range of habitats and play critical roles in sustaining healthy ecosystems that benefit human and nonhuman communities. Approximately 68% of primate species are threatened with extinction because of global pressures to convert their habitats for agricultural production and the extraction of natural resources. Here, we review the scientific literature and conduct a spatial analysis to assess the significance of Indigenous Peoples' lands in safeguarding primate biodiversity. We found that Indigenous Peoples' lands account for 30% of the primate range, and 71% of primate species inhabit these lands. As their range on these lands increases, primate species are less likely to be classified as threatened or have declining populations. Safeguarding Indigenous Peoples' lands, languages, and cultures represents our greatest chance to prevent the extinction of the world's primates.
Madagascar is a threatened global biodiversity hotspot and conservation priority, yet we lack broad-scale surveys to assess biodiversity across space and time. To fill this gap, we collated camera trap surveys, capturing species occurrences within Madagascar into a single standardized database. This data set includes nine distinct protected areas of Madagascar and encompasses 13 subprojects, 38 camera arrays, and 1156 sampling units (independent camera site per survey) within two important biodiversity eco-regions: western dry deciduous forest and eastern humid rainforest. Camera surveys were conducted from June 2007 to January 2021. The final data set includes 17 unique families of mammals (Bovidae, Canidae, Cheirogaleidae, Daubentoniidae, Equidae, Eupleridae, Felidae, Hominidae, Indriidae, Lemuridae, Lepilemuridae, Muridae, Nesomyidae, Pteropodidae, Soricidae, Suidae, Tenrecidae) comprising 45 species and 27 unique families of birds (Accipitridae, Acrocephalidae, Alcedinidae, Bernieridae, Brachypteraciidae, Caprimulgidae, Cisticolidae, Columbidae, Coraciidae, Corvidae, Cuculidae, Dicruridae, Mesitornithidae, Monarchidae, Motacillidae, Muscicapidae, Numididae, Phasianidae, Rallidae, Sarothruridae, Strigidae, Sturnidae, Sulidae, Threskiornithidae, Upupidae, Vangidae, Zosteropidae) comprising 58 species. Images were processed and verified by individual project data set creators and camera operation and species tables were then collated. The final product represents the first broad-scale freely available standardized formal faunal database for Madagascar. Data are available through this publication and at DOI: 10.5281/zenodo.5801806. These data will be useful for examining species-level and community-level trends in occurrence across space or time within Madagascar and globally, evaluating native and invasive species dynamics, and will aid in determining species conservation status and planning for at-risk species. There are no copyright restrictions; please cite this paper when using the data for publication.
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.
The spatial aggregation of species pairs often increases with the ecological similarity of the species involved. However, the way in which environmental conditions and anthropogenic activity affect the relationship between spatial aggregation and ecological similarity remains unknown despite the potential for spatial associations to affect species interactions, ecosystem function, and extinction risk. Given that human disturbance has been shown to both increase and decrease spatial associations among species pairs, ecological similarity may have a role in mediating these patterns. Here, we test the influences of habitat diversity, primary productivity, human population density, and species' ecological similarity based on functional traits (i.e., functional trait similarity) on spatial associations among tropical forest mammals. Large mammals are highly sensitive to anthropogenic change and therefore susceptible to changes in interspecific spatial associations. Using two-species occupancy models and camera trap data, we quantified the spatial overlap of 1216 species pairs from 13 tropical forest protected areas around the world. We found that the association between ecological similarity and interspecific species associations depended on surrounding human density. Specifically, aggregation of ecologically similar species was more than an order of magnitude stronger in landscapes with the highest human density compared to those with the lowest human density, even though all populations occurred within protected areas. Human-induced changes in interspecific spatial associations have been shown to alter top-down control by predators, increase disease transmission and increase local extinction rates. Our results indicate that anthropogenic effects on the distribution of wildlife within protected areas are already occurring and that impacts on species interactions, ecosystem functions, and extinction risk warrant further investigation.