Primate conservation: A public issue?

Nonhuman primates (primates) are one of the most endangered mammalian taxa in the world. In the Global North, primates are considered exotic species and, as such, humans' impact on primate conservation and responsibility to protect primates is often ignored. This view differs from the spectrum of relations and attitudes of humans that live in connection to primates, which can include viewing these animals as culturally/religiously significant, cohabitors of forests, nuisances, or sources of protein. While conservationists argue that primates deserve our protection, the conservation crisis facing primates is rarely framed as a public issue, in contrast to other global crises, such as climate change. However, over half of the world's human population lives within 100 km of primate habitat. Thus, humans and primates share the same environments. We suggest leveraging a holistic approach, such as One Health, that considers the interconnectedness of primates, humans, and their shared environments, through the lens of public anthropology. By approaching primate conservation as an intersectional issue that affects and is affected by humans, researchers and conservationists can identify strategies that simultaneously protect primates and address global inequities that frequently affect people in primate range countries. Reflexive research practices further allow academics to consider the broader impact of their ecological research through means such as publicly accessible dissemination of results, equitable capacity-building of high-quality personnel in primate range countries, and social activism. The use of inter-, multi-, and transdisciplinary concepts and methodology can address the intersectional challenges associated with implementing ethical and sustainable primate conservation measures.

Can cyclone exposure explain behavioural and demographic variation among lemur species?

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.

Context matters: Leveraging anthropology within one health.

Anthropologists develop long-term engagements with communities, animals, and the ecosystems they all share. This approach can provide important context that is necessary for One Health research, which may otherwise overlook the perspectives and lived experiences of community members. This paper presents two case studies that illustrate the importance of leveraging long-term, holistic, engagements with communities in moving the One Health concept forward. The first illustrates the complexity of understanding the health of people and animals within the context of environmental change in South India. The second provides insights into how the conservation of endangered species requires considering the entanglements of people, domestic animals, and the landscapes they share with wildlife in Madagascar. We demonstrate the value of integrating anthropological perspectives within interdisciplinary One Health research and interventions to better understand the complexity of systems.

Enter the Matrix: Use of Secondary Matrix by Mouse Lemurs.

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

Occurrence of lemurs in landscapes and their species-specific scale responses to habitat loss.

Studies on the impact of habitat loss on species occurrence consistently find that the amount of habitat (measured as patch area) is a major determinant of species occurrence at a patch-level. However, patch-level research may fail to detect important patterns and processes only observable at a landscape-level. A landscape-level approach that incorporates species-specific scale responses is needed to better understand what drives species occurrence. Our aim was to determine the landscape-level scale of effect of habitat amount on the occurrence of three species of nocturnal lemurs (Cheirogaleus medius, Microcebus murinus, and M. ravelobensis). We surveyed line transects to determine the occurrence of three lemur species within a fragmented landscape of deciduous dry forest and anthropogenic grassland in northwestern Madagascar. To determine the scale of effect of habitat loss on lemur occurrence, we compared logistic regression models of occurrence against habitat amount among eight different landscape scales using Akaike's Information Criterion values. We found differing scale responses among the lemurs in our study. Occurrence of C. medius responded to habitat amount at scales between 0.5-4 ha, M. murinus at scales between 1 and 4 ha and M. ravelobensis at scales between 0.125 and 4 ha. We suggest that the scale of effect for C. medius is mediated by their ability to hibernate. A relatively lower scale-response for Microcebus spp. likely reflect their omnivorous diet, small habitat requirements, and limited dispersal ability. Differences in scale responses between M. murinus and M. ravelobensis are likely a result of differing dispersal ability and responses to edge effects between these species. Our study is among the first on lemurs to show the value of a landscape-level approach when assessing the effects of habitat loss on species occurrence.

Species-area relationships of lemurs in a fragmented landscape in Madagascar.

We used species-area relationships (SARs) to investigate the effects of habitat loss on lemur biogeography. We measured species richness via visual surveys on line transects within 42 fragments of dry deciduous forest at the Ambanjabe field site in Ankarafantsika National Park, Madagascar. We measured human disturbance and habitat characteristics within 38 of the 42 fragments. We measured the distance between each fragment and the nearest settlement, continuous forest, and nearest neighboring fragment. We fit 10 candidate SAR models to the data using nonlinear least squares regression and compared them using Akaike's Information Criterion (AIC). To determine how habitat characteristics, as well as area, influenced species richness, we ran a hierarchical partitioning procedure to select which variables to include in generalized additive models (GAMs) and compared them using AIC. Contrary to expectations, we found that lemurs form convex SARs, without a "small island effect", and with the power model being the most likely SAR model. Although we found that four variables (area, survey effort, and total human disturbance, and mean tree height) independently contributed greater than 10% of the variation in lemur species richness, only area was included in the most likely model. We suggest that the power model was the most likely SAR model and our inability to detect a "small island effect" are the result of Microcebus spp. being edge tolerant and capable of dispersing through matrix, scale issues in the study design, and low γ-diversity in the landscape. However, more study is needed to determine what role human disturbance plays in influencing species richness in lemurs.

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

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