Geospatial and genomic tools for conserving the Critically Endangered blue-eyed black lemur (Eulemur flavifrons) and the sportive lemurs (genus Lepilemur)

Madagascar’s lemurs are the most endangered group of mammals in the world, with 94% of species threatened with extinction. Forest loss is one the greatest threat to these arboreal primates, but hunting, habitat degradation, and climate change also threaten their survival. Lemurs are a diverse group of more than 100 species; and their ecological traits shape how species respond to anthropogenic pressure. Incorporating knowledge of species’ ecological niches and evolutionary histories can contextualize threats and improve conservation assessments. In this dissertation, I investigate what constitutes suitable habitat for lemurs in light of the threats present, their sensitivity to forest fragmentation, their dispersal ability, and their ecological uniqueness. I obtained data about lemur distributions in two ways. First, I conducted field surveys of the Critically Endangered blue-eyed black lemur (Eulemur flavifrons), which only occurs in the ecotone between eastern rainforest and western dry forest in the Sahamalaza region. I also surveyed the range of sister species, the black lemur (E. macaco), which inhabits nearby eastern rainforest in the Manogarivo region. I focused on areas that have not been surveyed recently and on the poorly studied boundary between the species to collect observations from the breadth of these species’ ecological ranges. I also documented threats, including incursions into protected areas, and collected fecal samples to test whether whole genomes could be obtained noninvasively for analyses of local adaptation in these species. Second, I searched online databases and published literature for GPS localities for all species of lemur. I used these records, along with the ones collected in the field, to construct ecological niche models for nearly all species of lemur using Maxent. For the blue-eyed black lemur and the black lemur, I estimated the remaining area they can occupy based on these models and the threat survey data. Next, I examined the role of not just forest loss, but forest degradation, in determining where lemur species occur. I used high-resolution forest cover maps to determine lemurs’ tolerance for characteristics of degraded forest, including distance to the edge and mean patch size. I then limited species niche model to only intact, forested habitat. Lastly, using the sportive lemurs (genus Lepilemur) as an example, I evaluate how the inability to disperse across large rivers has influenced ecological niche diversity. I also examine what limited dispersal ability will mean for these species as climate change causes their ranges to shift. Field surveys in the Sahamalaza and Manongarivo regions revealed extensive threats to blue-eyed black lemurs, from traps to cattle incursions and fire. I found no evidence of sympatry, but did locate an undocumented population of E. flavifrons north of the Andranomalaza River. Madagascar National Parks (MNP) managed protected areas appear to have less human incursion than NGO-managed protected areas. Further investigation of the ecological distinctiveness of these species is possible via non-invasive methods: I sequenced whole genomes at 2.3x coverage from eight of the fecal samples collected during this study. While SNPs indicating a loss of function did not reveal any patterns, sequencing additional samples could make studies of local adaptation and population genetic diversity possible. At the regional scale, forest conversion is a grave threat to lemurs. When forest loss and degradation are considered in habitat models, lemur species have lost 51% of their habitat in the last 30 years. Proximity to a forest edge rendered more forested areas too degraded for lemurs than did mean patch size. This result is likely the influence of human contact nearer the forest edge. I recommend urgent support for reserves like Beanka, Tsimembo Forest, Ranobe PK 32, and Amoron’i Onilahy, which have highly suitable, intact forest for many lemur species. Spaces like these will be important for conserving the remarkable diversity within the sportive lemur clade. Though their distribution is largely explained by riverine barriers, I show a role for ecological niche divergence and local adaptation in accelerating allopatric speciation. These same rivers will limit their ability to track climatically suitable areas as climate change progresses: sportive lemurs as a group will lose nearly a quarter of their accessible habitat to climate change by the 2070s. While my results are focused on the particulars of lemur conservation in Madagascar, the methods I have presented here are broadly applicable to other threatened species. Piggybacking fecal sample collection onto rapid field surveys is straightforward. The possibility of obtaining whole genomes from non-invasive samples presents a new way to answer questions about local adaptation without risking injury to other arboreal study subjects, like Neotropical monkeys, or for elusive species like big cats. For threatened species, their climatic niche only dictates part of their distribution. The habitat quantification pipeline presented here takes advantage of thirty-five years of research in Madagascar to estimate species’ tolerance for forest fragmentation. While these records are impressive for primates, they are dwarfed by those available for passerines, through scientific literature and online repositories like eBird. By integrating field surveys, ecological niche modeling, and non-invasive genomics, we can begin to understand the complex threats facing species like lemurs and the options for ensuring their survival

Dietary flexibility of the greater bamboo lemur (Prolemur simus), a specialized feeder, in eastern Madagascar

The degree of dietary flexibility in primates is species specific; some incorporate a wider array of resources than others. Extreme interannual weather variability in Madagascar results in seasonal resource scarcity which has been linked to specialized behaviors in lemurs. Prolemur simus, for example, has been considered an obligate specialist on large culm bamboo with >60% of its diet composed of woody bamboos requiring morphological and physiological adaptations to process. Recent studies reported an ever‐expanding list of dietary items, suggesting that this species may not be an obligate specialist. However, long‐term quantitative feeding data are unavailable across this species’ range. To explore the dietary flexibility of P. simus, we collected data at two northern sites, Ambalafary and Sahavola, and one southern site, Vatovavy, from September 2010 to January 2016 and May 2017 to September 2018, respectively. In total, we recorded 4022 h of behavioral data using instantaneous sampling of adult males and females from one group in Ambalafary, and two groups each in Sahavola and Vatovavy. We recorded 45 plant species eaten by P. simus over 7 years. We also observed significant differences in seasonal dietary composition between study sites. In Ambalafary, bamboo was the most frequently observed resource consumed (92.2%); however, non‐bamboo resources comprised nearly one‐third of the diet of P. simus in Sahavola and over 60% in Vatovavy. Consumption of all bamboo resources increased during the dry season at Ambalafary and during the wet season at Vatovavy, but never exceeded non‐bamboo feeding at the latter. Culm pith feeding was only observed at Ambalafary, where it was more common during the dry season. We identify P. simus as a bamboo facultative specialist capable of adjusting its feeding behavior to its environment, indicating greater dietary flexibility than previously documented, which may enable the species to survive in increasingly degraded habitats

Tropical field stations yield high conservation return on investment

Conservation funding is currently limited; cost-effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID-19. We surveyed leaders of field stations across tropical regions that host primate research; 157 field stations in 56 countries responded. Respondents reported improved habitat quality and reduced hunting rates at over 80% of field stations and lower operational costs per km2 than protected areas, yet half of those surveyed have less funding now than in 2019. Spatial analyses support field station presence as reducing deforestation. These “earth observatories” provide a high return on investment; we advocate for increased support of field station programs and for governments to support their vital conservation efforts by investing accordingly.Additional co-authors: Ekwoge Abwe, Tanvir Ahmed, Marc Ancrenaz, Raphali R. Andriantsimanarilafy, Andie Ang, Filippo Aureli, Louise Barrett, Jacinta C. Beehner, Marcela E. Benítez, Bruna M. Bezerra, Júlio César Bicca-Marques, Dominique Bikaba, Robert Bitariho, Christophe Boesch, Laura M. Bolt, Ramesh Boonratana, Thomas M. Butynski, Gustavo R. Canale, Susana Carvalho, Colin A. Chapman, Dilip Chetry, Susan M. Cheyne, Marina Cords, Fanny M. Cornejo, Liliana Cortés-Ortiz, Camille N. Z. Coudrat, Margaret C. Crofoot, Drew T. Cronin, Alvine Dadjo, S. Chrystelle Dakpogan, Emmanuel Danquah, Tim R. B. Davenport, Yvonne A. de Jong, Stella de la Torre, Andrea Dempsey, Judeline C. Dimalibot, Rainer Dolch, Giuseppe Donati, Alejandro Estrada, Rassina A. Farassi, Peter J. Fashing, Eduardo Fernandez-Duque, Maria J. Ferreira da Silva, Julia Fischer, César F. Flores-Negrón, Barbara Fruth, Terence Fuh Neba, Lief Erikson Gamalo, Jörg U. Ganzhorn, Paul A. Garber, Smitha D. Gnanaolivu, Mary Katherine Gonder, Sery Ernest Gonedelé Bi, Benoit Goossens, Marcelo Gordo, Juan M. Guayasamin, Diana C. Guzmán-Caro, Andrew R. Halloran, Jessica A. Hartel, Eckhard W. Heymann, Russell A. Hill, Kimberley J. Hockings, Gottfried Hohmann, Naven Hon, Mariano G. Houngbédji, Michael A. Huffman, Rachel A. Ikemeh, Inaoyom Imong, Mitchell T. Irwin, Patrícia Izar, Leandro Jerusalinsky, Gladys Kalema-Zikusoka, Beth A. Kaplin, Peter M. Kappeler, Stanislaus M. Kivai, Cheryl D. Knott, Intanon Kolasartsanee, Kathelijne Koops, Martin M. Kowalewski, Deo Kujirakwinja, Ajith Kumar, Quyet K. Le, Rebecca J. Lewis, Aung Ko Lin, Andrés Link, Luz I. Loría, Menladi M. Lormie, Edward E. Louis Jr., Ngwe Lwin, Suchinda Malaivijitnond, Lesley Marisa, Gráinne M. McCabe, W. Scott McGraw, Addisu Mekonnen, Pedro G. Méndez-Carvajal, Tânia Minhós, David M. Montgomery, Citlalli Morelos-Juárez, David Morgan, Amancio Motove Etingüe, Papa Ibnou Ndiaye, K. Anne-Isola Nekaris, Nga Nguyen, Vincent Nijman, Radar Nishuli, Marilyn A. Norconk, Luciana I. Oklander, Rahayu Oktaviani, Julia Ostner, Emily Otali, Susan E. Perry, Eduardo J. Pinel Ramos, Leila M. Porter, Jill D. Pruetz, Anne E. Pusey, Helder L. Queiroz, Mónica A. Ramírez, Guy Hermas Randriatahina, Hoby Rasoanaivo, Jonah Ratsimbazafy, Joelisoa Ratsirarson, Josia Razafindramanana, Onja H. Razafindratsima, Vernon Reynolds, Rizaldi Rizaldi, Martha M. Robbins, Melissa E. Rodríguez, Marleny Rosales-Meda, Crickette M. Sanz, Dipto Sarkar, Anne Savage, Amy L. Schreier, Oliver Schülke, Gabriel H. Segniagbeto, Juan Carlos Serio-Silva, Arif Setiawan, John Seyjagat, Felipe E. Silva, Elizabeth M. Sinclair, Rebecca L. Smith, Denise Spaan, Fiona A. Stewart, Shirley C. Strum, Martin Surbeck, Magdalena S. Svensson, Mauricio Talebi, Luc Roscelin Tédonzong, Bernardo Urbani, João Valsecchi, Natalie Vasey, Erin R. Vogel, Robert B. Wallace, Janette Wallis, Siân Waters, Roman M. Wittig, Richard W. Wrangham, Patricia C. Wright, Russell A. Mittermeie

Do functional traits offset the effects of fragmentation? The case of large-bodied diurnal lemur species

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Do functional traits offset the effects of fragmentation? The case of large-bodied diurnal lemur species

Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation, are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large‐bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species’ distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore‐frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive folivores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape‐level reforestation efforts

Chromosome-length genome assemblies and cytogenomic analyses of pangolins reveal remarkable chromosome counts and plasticity

We report the first chromosome-length genome assemblies for three species in the mammalian order Pholidota: the white-bellied, Chinese, and Sunda pangolins. Surprisingly, we observe extraordinary karyotypic plasticity within this order and, in female white-bellied pangolins, the largest number of chromosomes reported in a Laurasiatherian mammal: 2n = 114. We perform the first karyotype analysis of an African pangolin and report a Y-autosome fusion in white-bellied pangolins, resulting in 2n = 113 for males. We employ a novel strategy to confirm the fusion and identify the autosome involved by finding the pseudoautosomal region (PAR) in the female genome assembly and analyzing the 3D contact frequency between PAR sequences and the rest of the genome in male and female white-bellied pangolins. Analyses of genetic variability show that white-bellied pangolins have intermediate levels of genome-wide heterozygosity relative to Chinese and Sunda pangolins, consistent with two moderate declines of historical effective population size. Our results reveal a remarkable feature of pangolin genome biology and highlight the need for further studies of these unique and endangered mammals

Tropical field stations yield high conservation return on investment

Conservation funding is currently limited; cost-effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID-19. We surveyed leaders of field stations across tropical regions that host primate research; 157 field stations in 56 countries responded. Respondents reported improved habitat quality and reduced hunting rates at over 80% of field stations and lower operational costs per km2 than protected areas, yet half of those surveyed have less funding now than in 2019. Spatial analyses support field station presence as reducing deforestation. These ‘earth observatories’ provide a high return on investment; we advocate for increased support of field station programs and for governments to support their vital conservation efforts by investing accordingly