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.

Infant nest and stash sites of variegated lemurs (Varecia rubra): The extended phenotype.

Very few primate species give birth to litters and build nests in which to care for them. Those that do are small-bodied, nocturnal, and solitary. Variegated lemurs are exceptional in that they bear litters in arboreal nests, yet are relatively large-bodied, day-active, and gregarious. Furthermore, they raise their young cooperatively and practice absentee parenting; non-clinging young are transported orally and periodically stashed in arboreal spots that are supportive, sheltered, and usually concealed. Following birth, infant nest and stash trees were mapped, measured, and taxonomically identified in a population of red variegated lemurs in Masoala National Park. About 40 trees were used per litter for nesting and stashing young in adjacent, non-overlapping core areas within the community. These were the largest trees in the forest, even larger than those used for feeding. Furthermore, most occur in valleys and are laced with lianas, creating sites that buffer young from predation, accidental falls, and to some degree, thermal stress. In combination, the number of nest and stash trees used per litter, their characteristics, and their geo-spatial arrangement indicate that such sites are both select and limited in the landscape, exposing the dependence of red variegated lemurs on intact forest canopies for raising non-clinging young within the context of an absentee parenting system. Nest and stash sites are in effect Varecia's extended phenotype. Logging of large trees in Madagascar's eastern rain forests is considered a major factor resulting in local extinctions of variegated lemurs because they rely heavily upon large, mature trees for fruit. However, this study suggests that removal of large trees may more directly precipitate local extinctions by impeding their ability to reproduce. Long-term survival of red variegated lemurs will depend upon efforts to end harmful timber extraction in its remaining stronghold, the Masoala Peninsula.

Introducing IsoMad, a compilation of isotopic datasets for Madagascar.

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.

Madagascar Terrestrial Camera Survey Database 2021: A collation of protected forest camera surveys from 2007-2021.

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.

The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report.

Captive studies have shown that ruffed lemurs (Varecia) have an unusual suite of reproductive traits combined with extremely high maternal reproductive costs. These traits include the bearing of litters, nesting of altricial young, and absentee parenting. To characterize the breeding system of this enigmatic lemur, reproductive traits must be contextualized in the wild. Here, I provide a preliminary report of mating and infant care in one community of wild red ruffed lemurs (Varecia rubra). Observations span a 15-month period covering two birth seasons and one mating season on the Masoala Peninsula, Madagascar. Factors that are not possible to replicate in captivity are reported, such as mating pattern, natality and mortality rates, the location of nests within the home range, and the structuring of infant care within a natural community. V. rubra at Andranobe have a fission-fusion, multifemale-multimale grouping pattern and a polygamous mating system. They do not mate monogamously or live strictly in family-based groups as suggested by previous workers. During the first 2 months of life, nests and infant stashing localities are situated within each mother's respective core area, and inhabitants of each core area within the communal home range provide care for young. As part of their absentee parenting system, infants are left in concealed, protected, and supportive spots high in the canopy, while mothers travel distantly. This practice is termed 'infant stashing'. Alloparenting appears to be an integral part of V. rubra's overall reproductive strategy in the wild, as it was performed by all age-sex classes. Among the alloparental behaviors observed were infant guarding, co-stashing, infant transport, and allonursing. Alloparenting and absentee parenting may mitigate high maternal reproductive costs. Furthermore, V. rubra may have a breeding system in which genetic partners (i.e., mating partners) do not always correspond to infant care-providers. Combined with recently available information on the behavioral ecology of wild ruffed lemurs, this preliminary report suggests directions for in-depth studies on Varecia's breeding system.

Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala national park.

The current range of the red ruffed lemur (Varecia rubra) population is primarily restricted to forests of the Masoala Peninsula on the northeastern coast of Madagascar. Whereas much of the peninsula is protected as Masoala National Park, parts of the forest are at risk from anthropogenic pressures and habitat fragmentation. We sampled 32 individual red ruffed lemur from two sites: Ambatoledama (DAMA), a narrow forest corridor across an area of degraded habitat connecting larger blocks of forest in the northwestern reaches of the park, and Masiaposa (MAS) forest, a largely pristine forest on the lower western side of the peninsula. Population genetic parameters were estimated for these two populations employing 15 microsatellite loci derived from the V. variegata genome. We found that by exceeding the expected heterozygosity at mutation-drift equilibrium, the DAMA population has undergone a recent population bottleneck. Population structure analysis detected individuals harboring genotypic admixture of the DAMA genetic cluster in the MAS population, suggesting a possibility of unilateral gene flow or movement between these populations.

New developments in the behavioral ecology and conservation of ruffed lemurs (Varecia).

The papers in this issue were presented at a symposium during the 25th Annual Meeting of the American Society of Primatologists held in Oklahoma City, Oklahoma, in June 2002. This symposium brought together many of the scientists who have contributed to our knowledge of ruffed lemur ecology, behavior, and conservation in the past decade. One objective was to share and compare key findings about ruffed lemurs (Varecia) resulting from long-term field studies at various sites in Madagascar. A second objective was to cross-fertilize work being done in the wild with that being done in captivity, with the aim of advancing a common conservation mission for this critically endangered genus. Varecia is a prime candidate for synthetic assessments such as these because it has now been studied in both the northern and southern reaches of its geographic range, and has also been the focus of a captive-to-wild reinforcement project. The papers in this issue contribute to 1) the establishment of reference ranges for a suite of physiological parameters in healthy wild Varecia populations; 2) environmental enrichment aimed at preserving species-typical behaviors in captivity; 3) an understanding of how forest structure, floristic composition, and fruiting phenology in areas with differing disturbance histories correlate with the natural occurrence and abundance of Varecia; 4) primary knowledge concerning dominance relations between the sexes and group leadership in wild Varecia; and 5) primary knowledge concerning how wild Varecia, with their unusual reproductive pattern and heavy reliance on fruit, modulate their activity budgets seasonally and in tandem with reproductive stages.

Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: seasonality and reproductive energetics.

The activity budgets and daily activity rhythms of Varecia rubra were examined over an annual cycle according to season and reproductive stage. Given the relatively high reproductive costs and patchy food resources of this species, I predicted that V. rubra would 1) travel less and feed more during seasonal resource scarcity in an attempt to maintain energy balance, and 2) show sex differences in activity budgets due to differing reproductive investment. Contrary to the first prediction, V. rubra does not increase feeding time during seasonal food scarcity; rather, females feed for a consistent amount of time in every season, whereas males feed most during the resource-rich, hot dry season. The results are consistent with other predictions: V. rubra travels less in the resource-scarce cold rainy season, and there are some pronounced sex differences, with females feeding more and resting less than males in every season and in every reproductive stage except gestation. However, there are also some provocative similarities between the sexes when activity budgets are examined by reproductive stage. During gestation, female and male activity budgets do not differ and appear geared toward energy accumulation: both sexes feed and rest extensively and travel least during this stage. During lactation, activity budgets are geared toward high energy expenditure: both sexes travel most and in equal measure, and rest least, although it remains the case that females feed more and rest less than males. These similarities between female and male activity budgets appear related to cooperative infant care. The high energetic costs of reproduction in V. rubra females may require that they allot more time to feeding year round, and that their overall activity budget be more directly responsive to seasonal climate change, seasonal food distribution, and reproductive schedules.

Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns.

Based on a year-long field study in northeastern Madagascar, I summarize annual patterns of niche use (food patch size, diet, forest height, and forest site) in two sympatric lemurs, Varecia variegata rubra and Eulemur fulvus albifrons. Furthermore, I examine intraspecific patterns of niche use according to sex, season, and reproductive stage in these two lemurs that differ in terms of energetic investment in reproduction. Lemurs as a group provide a special opportunity to test hypotheses concerning sex differences in niche use. Due to their body size monomorphism and seasonal, synchronous pattern of breeding, it is possible to directly evaluate whether sex differences in diet reflect high energetic investment in reproduction by females. Results confirm the hypothesis that intraspecific variation in niche use (e.g., sex differences, seasonal differences) would be more pronounced in V. v. rubra than in E. f. albifrons, due in large measure to the former's relatively high energetic investment in reproduction: 1a) Dietary sex differences in V. v. rubra are most pronounced during costly reproductive stages and involve acquisition of low-fiber, high-protein plant foods. Females of both species consume more seasonally available low-fiber protein (young leaves, flowers) relative to conspecific males during the hot dry season, but only in V. v. rubra females is this pattern also evident during gestation and lactation. 1b) The diets of female V. v. rubra and female E. f. albifrons are more similar to each other than are the diets of conspecific males and females in the case of V. v. rubra. This is not uniformly the case for female E. f. albifrons. This finding confirms a hypothesis put forward in Vasey ([2000] Am J Phys Anthropol 112:411-431) that energetic requirements of reproductive females drive niche separation more than do the energetic requirements of males. 1c) Both species synchronize most or all of lactation with seasonal food abundance and diversity. E. f. albifrons shows a more protracted period of synchrony, and this may contribute to its wide biogeographic distribution in Madagascar. 2) Sex differences and seasonal differences in microhabitat use reflect intraspecific patterns of thermoregulation, predator avoidance, and in the case of V. v. rubra, reproduction. One important factor selecting for body size monomorphism in lemurs appears to be the tight synchrony between lactation and periods of food abundance afforded by annual, seasonal breeding.

Circadian rhythms in diet and habitat use in red ruffed lemurs (Varecia rubra) and white-fronted brown lemurs (Eulemur fulvus albifrons).

Daily variation in niche use among vertebrates is attributed to a variety of factors, including thermoregulatory, reproductive, and nutritional requirements. Lemuriform primates exhibit many behavioral and physiological adaptations related to thermoregulation and sharp, seasonal reproduction, yet they have rarely been subjects of a quantitative analysis of circadian (or daily) rhythms in niche use. In this study, I document daily rhythms in diet and microhabitat use over an annual cycle in two sympatric, frugivorous lemurs, Varecia rubra and Eulemur fulvus albifrons. Data on diet, forest site, and forest height were recorded at 5-min time points on focal animals and divided into three time blocks for analysis (06:00-10:00 hr, 10:00-14:00 hr, and 14:00-18:00 hr). I employed multivariate tests of independence to examine daily rhythms in diet and microhabitat use according to sex, season, and reproductive stage. Throughout the day, V. rubra is frugivorous and dwells in the upper canopy, with notable departures (especially for females) during the hot seasons, gestation, and lactation. E. f. albifrons has heterogeneous daily rhythms of food choice and microhabitat use, particularly across seasons, and both sexes are equally variable. These daily rhythms in diet and microhabitat use appear related to thermoregulatory and nutritional requirements, seasonal food availability and circadian rhythms of plant (and possibly insect) palatability, predator avoidance tactics, and in the case of Varecia, to reproduction. Daily rhythms of food choice in V. rubra support two previously suggested hypotheses explaining why primates consume more nonfruit items late in the day, whereas those of E. f. albifrons are too variable to lend support to these hypotheses.