Arboreal mouse lemurs discovered sleeping in a burrow on the ground.

Finding sleeping sites is important for the fitness of many mammal species. Like most nonhuman primates, Madagascar's mouse lemurs (genus: Microcebus) are thought to exclusively use arboreal sleeping sites. The rufous mouse lemurs (Microcebus rufus) in Ranomafana National Park (southeastern Madagascar) have always been documented to sleep in either tree holes or leaf nests. However, in our recent field expedition, we observed, with the help of telemetry technologies, an unprecedented event of M. rufus sleeping in a burrow on the rainforest ground, curled up with a very slow heartbeat. Thus far, such behavior has not been observed in any other Microcebus species but is common in high-altitude dwarf lemurs (genus: Cheirogaleus), a closely related genus to the mouse lemurs. We believe that this discovery could illustrate an ecophysiological response strategy to habitat changes, which warrants further investigation.

A set of principles and practical suggestions for equitable fieldwork in biology.

Field biology is an area of research that involves working directly with living organisms in situ through a practice known as "fieldwork." Conducting fieldwork often requires complex logistical planning within multiregional or multinational teams, interacting with local communities at field sites, and collaborative research led by one or a few of the core team members. However, existing power imbalances stemming from geopolitical history, discrimination, and professional position, among other factors, perpetuate inequities when conducting these research endeavors. After reflecting on our own research programs, we propose four general principles to guide equitable, inclusive, ethical, and safe practices in field biology: be collaborative, be respectful, be legal, and be safe. Although many biologists already structure their field programs around these principles or similar values, executing equitable research practices can prove challenging and requires careful consideration, especially by those in positions with relatively greater privilege. Based on experiences and input from a diverse group of global collaborators, we provide suggestions for action-oriented approaches to make field biology more equitable, with particular attention to how those with greater privilege can contribute. While we acknowledge that not all suggestions will be applicable to every institution or program, we hope that they will generate discussions and provide a baseline for training in proactive, equitable fieldwork practices.

Advancing an interdisciplinary framework to study seed dispersal ecology.

Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant's life history and environmental variability that ultimately influences a population's ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive.

There is growing realization that intraspecific variation in seed dispersal can have important ecological and evolutionary consequences. However, we do not have a good understanding of the drivers or causes of intraspecific variation in dispersal, how strong an effect these drivers have, and how widespread they are across dispersal modes. As a first step to developing a better understanding, we present a broad, but not exhaustive, review of what is known about the drivers of intraspecific variation in seed dispersal, and what remains uncertain. We start by decomposing 'drivers of intraspecific variation in seed dispersal' into intrinsic drivers (i.e. variation in traits of individual plants) and extrinsic drivers (i.e. variation in ecological context). For intrinsic traits, we further decompose intraspecific variation into variation among individuals and variation of trait values within individuals. We then review our understanding of the major intrinsic and extrinsic drivers of intraspecific variation in seed dispersal, with an emphasis on variation among individuals. Crop size is the best-supported and best-understood intrinsic driver of variation across dispersal modes; overall, more seeds are dispersed as more seeds are produced, even in cases where per seed dispersal rates decline. Fruit/seed size is the second most widely studied intrinsic driver, and is also relevant to a broad range of seed dispersal modes. Remaining intrinsic drivers are poorly understood, and range from effects that are probably widespread, such as plant height, to drivers that are most likely sporadic, such as fruit or seed colour polymorphism. Primary extrinsic drivers of variation in seed dispersal include local environmental conditions and habitat structure. Finally, we present a selection of outstanding questions as a starting point to advance our understanding of individual variation in seed dispersal.

The total dispersal kernel: a review and future directions.

The distribution and abundance of plants across the world depends in part on their ability to move, which is commonly characterized by a dispersal kernel. For seeds, the total dispersal kernel (TDK) describes the combined influence of all primary, secondary and higher-order dispersal vectors on the overall dispersal kernel for a plant individual, population, species or community. Understanding the role of each vector within the TDK, and their combined influence on the TDK, is critically important for being able to predict plant responses to a changing biotic or abiotic environment. In addition, fully characterizing the TDK by including all vectors may affect predictions of population spread. Here, we review existing research on the TDK and discuss advances in empirical, conceptual modelling and statistical approaches that will facilitate broader application. The concept is simple, but few examples of well-characterized TDKs exist. We find that significant empirical challenges exist, as many studies do not account for all dispersal vectors (e.g. gravity, higher-order dispersal vectors), inadequately measure or estimate long-distance dispersal resulting from multiple vectors and/or neglect spatial heterogeneity and context dependence. Existing mathematical and conceptual modelling approaches and statistical methods allow fitting individual dispersal kernels and combining them to form a TDK; these will perform best if robust prior information is available. We recommend a modelling cycle to parameterize TDKs, where empirical data inform models, which in turn inform additional data collection. Finally, we recommend that the TDK concept be extended to account for not only where seeds land, but also how that location affects the likelihood of establishing and producing a reproductive adult, i.e. the total effective dispersal kernel.

MADA: Malagasy Animal trait Data Archive.

Species are characterized by their behavioral, physiological, and ecological attributes, which determine their role in ecosystems. In turn, ecosystems and their functions are defined by the species that inhabit them. Thus, evaluating the functional diversity and distributions of species is of utmost importance to studies of biogeography, community ecology, macroevolution, and conservation. The functional diversity of species are determined by traits such as diet, foraging strata, trophic level, activity cycle, litter size, generation length, habitat breadth, and body mass. While there has been a recent growth of information regarding the vertebrate taxa of Madagascar, this information is not always easy to access (non-digitized), and is often fragmented by taxon, location, trait, or combinations thereof. Here, we present the Malagasy Animal trait Data Archive (MADA), a compilation of these and other functional traits, representing the ecological and geographical diversity of all 214 extant mammal and 242 bird species of Madagascar. Data were collected from extensive literature reviews. This Archive is currently limited by select cases of missing data, errors, and uncertainty in the literature; however, it represents the most comprehensive collection of functional trait data of Malagasy mammals and birds to date. The structure of the database allows for different levels of information (and specificity) in each entry and organization by taxon, range, bioclimate, and trait. MADA will be continuously updated as new data become available. Potential uses of MADA include ecological research on the trait or trophic structure of communities, inquiries regarding the mechanisms of community assembly, comparative studies of functionally (dis)similar species, and conservation efforts concerned with the loss of ecosystem function. Madagascar is simultaneously home to one of the most exclusive, diverse, and endangered faunas of the world, making MADA a uniquely valuable resource for biodiversity science and conservation. No copyright restrictions are associated with this dataset. We would appreciate that researchers cite this paper if using all or part of the datasets.

Frugivores bias seed-adult tree associations through nonrandom seed dispersal: a phylogenetic approach.

Frugivores are the main seed dispersers in many ecosystems, such that behaviorally driven, nonrandom patterns of seed dispersal are a common process; but patterns are poorly understood. Characterizing these patterns may be essential for understanding spatial organization of fruiting trees and drivers of seed-dispersal limitation in biodiverse forests. To address this, we studied resulting spatial associations between dispersed seeds and adult tree neighbors in a diverse rainforest in Madagascar, using a temporal and phylogenetic approach. Data show that by using fruiting trees as seed-dispersal foci, frugivores bias seed dispersal under conspecific adults and under heterospecific trees that share dispersers and fruiting time with the dispersed species. Frugivore-mediated seed dispersal also resulted in nonrandom phylogenetic associations of dispersed seeds with their nearest adult neighbors, in nine out of the 16 months of our study. However, these nonrandom phylogenetic associations fluctuated unpredictably over time, ranging from clustered to overdispersed. The spatial and phylogenetic template of seed dispersal did not translate to similar patterns of association in adult tree neighborhoods, suggesting the importance of post-dispersal processes in structuring plant communities. Results suggest that frugivore-mediated seed dispersal is important for structuring early stages of plant-plant associations, setting the template for post-dispersal processes that influence ultimate patterns of plant recruitment. Importantly, if biased patterns of dispersal are common in other systems, frugivores may promote tree coexistence in biodiverse forests by limiting the frequency and diversity of heterospecific interactions of seeds they disperse.

Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment.

Directed dispersal is defined as enhanced dispersal of seeds into suitable microhabitats, resulting in higher recruitment than if seeds were dispersed randomly. While this constitutes one of the main explanations for the adaptive value of frugivore-mediated seed dispersal, the generality of this advantage has received little study, particularly when multiple dispersers are involved. We used probability recruitment models of a long-lived rainforest tree in Madagascar to compare recruitment success under dispersal by multiple frugivores, no dispersal, and random dispersal. Models were parameterized using a three-year recruitment experiment and observational data of dispersal events by three frugivorous lemur species that commonly disperse its seeds. Frugivore-mediated seed dispersal was nonrandom with respect to canopy cover and increased modeled per-seed sapling recruitment fourfold compared to no dispersal. Seeds dispersed by one frugivore, Eulemur rubriventer, had higher modeled recruitment probability than seeds dispersed randomly. However, as a group, our models suggest that seeds dispersed by lemurs would have lower recruitment than if dispersal were random. Results demonstrate the importance of evaluating the contribution of multiple frugivores to plant recruitment for understanding plant population dynamics and the ecological and evolutionary significance of seed dispersal.

Frugivory and seed dispersal patterns of the red-ruffed lemur, Varecia rubra, at a forest restoration site in Masoala National Park, Madagascar.

Frugivorous primates can play a critical role in the regeneration of degraded habitats by dispersing seeds of their food plants. We studied the diet and seed dispersal patterns of 3 groups of habituated red-ruffed lemurs (Varecia rubra) in a rain forest restoration site in Masoala National Park, Madagascar, to assess the species' seed dispersal effectiveness. Fruits accounted for 61% of the diet, with an average foraging time of 10 min per fruit patch per day. Seeds from 75% of the consumed fruit species were recovered in the collected V. rubra feces. We traced the potential parent plants of 20 dispersed-seed species to calculate a gut passage range (63-423 min; mean = 225, n = 35). The median seed dispersal distance from the potential parent plant was 48 m (mean = 83 m, range 0-568 m, n = 194). The home ranges of 2 of the 3 groups overlapped with the regenerating forest parcels. Although 92% of fecal samples with seeds were dispersed into the undisturbed forest, V. rubra fed on the fruits of the non-native pioneer shrub Clidemia hirta, while also dispersing native and non-native seed species into the regenerating forest parcels.

Patterns of movement and seed dispersal by three lemur species.

We combined data on gut-passage times, feeding, and movement to explore the patterns of seed dispersal by Eulemur rubriventer, Eulemur rufrifrons, and Varecia variegata editorum lemurs in Ranomafana National Park, Madagascar. These lemur species deposited less than half of their consumed seeds >100 m away from conspecific trees (40-50%). Long-distance dispersal (>500 m) was rare and average dispersal distances were short relative to those reported of similar-sized haplorrhine primates. The three lemur species showed no significant differences in mean seed-dispersal distances. However, they differed in the shape of their frequency distributions of seed-dispersal distances as a result of differences in how they moved through their habitats. The short distances of seed dispersal we observed and the depauperate frugivorous fauna in Madagascar suggest seed-dispersal may be more limited than in other tropical forests with important implications for plant-community dynamics, biodiversity maintenance, and restoration efforts in Madagascar.