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.

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.

Habitat use by the island lemurs of Nosy Be, Madagascar.

Madagascar's lemurs are threatened by forest loss, fragmentation, and degradation. Many species use flexible behaviors to survive in degraded habitat, but their ability to persist in very small areas may be limited. Insular lemurs, like those found on Nosy Be, an island off the northwestern coast of Madagascar, are at heightened risk of sudden population declines and extirpation. Nosy Be is home to two Critically Endangered species-the endemic Nosy Be sportive lemur (Lepilemur tymerlachsoni) and Claire's mouse lemur (Microcebus mamiratra)-as well as the Endangered black lemur (Eulemur macaco). Most of the remaining forest on Nosy Be is protected by the 862-ha Lokobe National Park. To document how Nosy Be lemurs use their restricted habitat, we conducted vegetation and reconnaissance surveys on 53 transects in and around Lokobe. We collected data on tree size, canopy cover, understory visibility, and elevation for 248 lemur sightings. We used a spatially explicit, multi-species occupancy model to investigate which forest-structure variables are important to lemurs. Our results represent some of the first data on habitat use by insular lemurs. Black lemurs preferred significantly larger trees and areas with less dense understory. They also occurred significantly less outside of Lokobe National Park, even when accounting for sampling effort and geography. The distributions of the sportive and mouse lemurs were not related to the forest structure variables we documented, but they did negatively predict each other-perhaps because their habitat requirements differ. These results also underscore the importance of the national park to protecting the black lemur population on Nosy Be and raise questions about what factors do influence the distribution of Nosy Be's smaller lemurs. Close monitoring is needed to prevent these populations and the ecosystem services they provide from disappearing, as have other island lemurs.

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.

Population structure and demographic history of two highly-trafficked species of pangolin in the Congo Basin.

African pangolins are hunted for their meat and for use in local traditional medicine, as well as for their scales, which are trafficked internationally, especially to growing Asian markets. Pangolin's population genetic structure can be used to trace the geographic origins of trafficked scales, but substantial sampling gaps across pangolins' ranges hinder these efforts. In this study, we documented population structure and dynamics in the two species of African pangolin, the white-bellied pangolin (Phataginus tricuspis) and the giant pangolin (Smutsia gigantea) in the underexplored Republic of Congo. Using the mitochondrial control region and two nuclear markers (beta-fibrinogen and titin), we identified high genetic diversity in both species. We document a distinct mitochondrial lineage of the white-bellied pangolin, which was most likely shaped by river barriers together with dynamics of forest refugia related to the climatic shifts during the Pleistocene. We detected population growth in the white-bellied pangolin coinciding with a dry period during the Pleistocene, suggesting some ability for this typically forest-dwelling species to persist under diverse environmental conditions. Using landscape genetics, we found all but one of the pangolins we sampled at bush meat markets originated locally. A single individual appeared to have been imported to Congo from Cameroon. These findings significantly contribute to our understanding of pangolin population biology and local trade dynamics. In addition, our data from a previously unstudied part of pangolins' ranges will help us to better understand international wildlife trafficking patterns and to target conservation and protection strategies for these highly vulnerable species.

Assessing evidence on the impacts of nature-based interventions for climate change mitigation: a systematic map of primary and secondary research from subtropical and tropical terrestrial regions.

BACKGROUND: Nature-based interventions (NbIs) for climate change mitigation include a diverse set of interventions aimed at conserving, restoring, and/or managing natural and modified ecosystems to improve their ability to store and sequester carbon and avoid greenhouse gas (GHG) emissions. Recent projections estimate that terrestrial NbIs can lead to more than one-third of the climate change mitigation necessary to meet the Paris Climate Agreement by 2030. Further, these interventions can provide co-benefits in the form of social and ecological outcomes. Despite growing recognition of the potential benefits, a clear characterization of the distribution and occurrence of evidence which supports linkages between different types of NbIs and outcomes for climate change mitigation, ecosystems, and people remains poorly understood. METHODS: This systematic map assesses the evidence base on the links between NbIs and climate change mitigation, social, and ecological outcomes in tropical and subtropical terrestrial regions. We searched three bibliographic databases, 65 organization websites, and conducted backward citation chasing within 39 existing evidence syntheses to identify relevant articles. Additionally, we reached out to key informants for additional sources of evidence. We then used machine learning to rank returned results by relevance at the title and abstract stage and manually screened for inclusion using predefined criteria at the title, abstract, and full text stages. We extracted relevant meta-data from included articles using an a priori coding scheme. Lastly, we conducted a targeted, complementary search to identify relevant review and synthesis articles to provide broader context for the findings of the systematic map. REVIEW FINDINGS: We included 948 articles in this systematic map. Most of the evidence base (56%) examined links between protection, natural resource management, and restoration interventions with changes to 'proxy' outcomes for climate change mitigation (changes to land condition, land cover, and/or land use). Other areas with high occurrence of articles included linkages between interventions within natural resource management and trees in croplands categories and changes to aboveground carbon storage and/or sequestration (17% of articles). A key knowledge gap was on measured changes in GHG emissions across all intervention types (6% of articles). Overall, articles in the evidence base did not often assess changes in co-benefits alongside direct or indirect changes for climate change mitigation (32%). In most cases, the evidence base contained studies which did not explicitly test for causal linkages using appropriate experimental or quasi-experimental designs. CONCLUSIONS: The evidence base for NbIs is significant and growing; however, key gaps in knowledge hamper the ability to inform ongoing and future investment and implementation at scale. More comprehensive evidence is needed to support causal inference between NbIs and direct outcomes for climate change mitigation to better determine additionality, permanence, leakage, and other unintended consequences. Similarly, priorities emerging from this map include the need for coordinated and harmonized efforts to collect diverse data types to better understand whether and how other outcomes (e.g. social, ecological) of NbIs can be achieved synergistically with mitigation objectives. Understanding potential benefits and trade-offs of NbIs is particularly urgent to inform rapidly expanding carbon markets for nature.

Genomic analyses reveal poaching hotspots and illegal trade in pangolins from Africa to Asia.

The white-bellied pangolin (Phataginus tricuspis) is the world's most trafficked mammal and is at risk of extinction. Reducing the illegal wildlife trade requires an understanding of its origins. Using a genomic approach for tracing confiscations and analyzing 111 samples collected from known geographic localities in Africa and 643 seized scales from Asia between 2012 and 2018, we found that poaching pressures shifted over time from West to Central Africa. Recently, Cameroon's southern border has emerged as a site of intense poaching. Using data from seizures representing nearly 1 million African pangolins, we identified Nigeria as one important hub for trafficking, where scales are amassed and transshipped to markets in Asia. This origin-to-destination approach offers new opportunities to disrupt the illegal wildlife trade and to guide anti-trafficking measures.

Nuclear and Mitochondrial Phylogenomics of the Sifakas Reveal Cryptic Variation in the Diademed Sifaka.

The most comprehensive phylogenomic reconstruction to date was generated on all nominal taxa within the lemur genus Propithecus. Over 200 wild-caught individuals were included in this study to evaluate the intra and interspecific relationships across this genus. Ultraconserved Elements (UCEs) resulted in well-supported phylogenomic trees. Complete mitochondrial genomes (CMGs) largely agreed with the UCEs, except where a mitochondrial introgression was detected between one clade of the diademed sifaka (Propithecus diadema) and the Milne-Edwards sifaka (P. edwardsi). Additionally, the crowned (P. coronatus) and Von der Decken's (P. deckeni) sifakas belonged to a single admixed lineage from UCEs. Further sampling across these two species is warranted to determine if our sampling represents a hybrid zone. P. diadema recovered two well-supported clades, which were dated and estimated as being ancient as the split between the Perrier's (P. perrierii) and silky (P. candidus) sifakas. The reconstructed demographic history of the two clades also varied over time. We then modeled the modern ecological niches of the two cryptic P. diadema clades and found that they were significantly diverged (p < 0.01). These ecological differences result in a very limited zone of geographic overlap for the P. diadema clades (<60 km2). Niche models also revealed that the Onive River acts as a potential barrier to dispersal between P. diadema and P. edwardsi. Further taxonomic work is required on P. diadema to determine if its taxonomic status should be revised. This first genomic evaluation of the genus resolved the relationships between the taxa and the recovered cryptic diversity within one species.

What evidence exists on the links between natural climate solutions and climate change mitigation outcomes in subtropical and tropical terrestrial regions? A systematic map protocol.

Background: Natural climate solutions (NCS)-actions to conserve, restore, and modify natural and modified ecosystems to increase carbon storage or avoid greenhouse gas (GHG) emissions-are increasingly regarded as important pathways for climate change mitigation, while contributing to our global conservation efforts, overall planetary resilience, and sustainable development goals. Recently, projections posit that terrestrial-based NCS can potentially capture or avoid the emission of at least 11 Gt (gigatons) of carbon dioxide equivalent a year, or roughly encompassing one third of the emissions reductions needed to meet the Paris Climate Agreement goals by 2030. NCS interventions also purport to provide co-benefits such as improved productivity and livelihoods from sustainable natural resource management, protection of locally and culturally important natural areas, and downstream climate adaptation benefits. Attention on implementing NCS to address climate change across global and national agendas has grown-however, clear understanding of which types of NCS interventions have undergone substantial study versus those that require additional evidence is still lacking. This study aims to conduct a systematic map to collate and describe the current state, distribution, and methods used for evidence on the links between NCS interventions and climate change mitigation outcomes within tropical and sub-tropical terrestrial ecosystems. Results of this study can be used to inform program and policy design and highlight critical knowledge gaps where future evaluation, research, and syntheses are needed. Methods: To develop this systematic map, we will search two bibliographic databases (including 11 indices) and 67 organization websites, backward citation chase from 39 existing evidence syntheses, and solicit information from key informants. All searches will be conducted in English and encompass subtropical and tropical terrestrial ecosystems (forests, grasslands, mangroves, agricultural areas). Search results will be screened at title and abstract, and full text levels, recording both the number of excluded articles and reasons for exclusion. Key meta-data from included articles will be coded and reported in a narrative review that will summarize trends in the evidence base, assess gaps in knowledge, and provide insights for policy, practice, and research. The data from this systematic map will be made open access. Supplementary Information: The online version contains supplementary material available at 10.1186/s13750-022-00268-w.

What evidence exists on the links between natural climate solutions and climate change mitigation outcomes in subtropical and tropical terrestrial regions? A systematic map protocol.

BACKGROUND: Natural climate solutions (NCS)-actions to conserve, restore, and modify natural and modified ecosystems to increase carbon storage or avoid greenhouse gas (GHG) emissions-are increasingly regarded as important pathways for climate change mitigation, while contributing to our global conservation efforts, overall planetary resilience, and sustainable development goals. Recently, projections posit that terrestrial-based NCS can potentially capture or avoid the emission of at least 11 Gt (gigatons) of carbon dioxide equivalent a year, or roughly encompassing one third of the emissions reductions needed to meet the Paris Climate Agreement goals by 2030. NCS interventions also purport to provide co-benefits such as improved productivity and livelihoods from sustainable natural resource management, protection of locally and culturally important natural areas, and downstream climate adaptation benefits. Attention on implementing NCS to address climate change across global and national agendas has grown-however, clear understanding of which types of NCS interventions have undergone substantial study versus those that require additional evidence is still lacking. This study aims to conduct a systematic map to collate and describe the current state, distribution, and methods used for evidence on the links between NCS interventions and climate change mitigation outcomes within tropical and sub-tropical terrestrial ecosystems. Results of this study can be used to inform program and policy design and highlight critical knowledge gaps where future evaluation, research, and syntheses are needed. METHODS: To develop this systematic map, we will search two bibliographic databases (including 11 indices) and 67 organization websites, backward citation chase from 39 existing evidence syntheses, and solicit information from key informants. All searches will be conducted in English and encompass subtropical and tropical terrestrial ecosystems (forests, grasslands, mangroves, agricultural areas). Search results will be screened at title and abstract, and full text levels, recording both the number of excluded articles and reasons for exclusion. Key meta-data from included articles will be coded and reported in a narrative review that will summarize trends in the evidence base, assess gaps in knowledge, and provide insights for policy, practice, and research. The data from this systematic map will be made open access.

Perseverance and food sharing among closely affiliated female chimpanzees.

Chimpanzees (Pan troglodytes) have been frequently observed to share food with one another, with numerous hypotheses proposed to explain why. These often focus on reciprocity exchanges for social benefits (e.g., food for grooming, food for sex, affiliation, kinship, and dominance rank) as well as sharing based on begging and deterring harassment. Although previous studies have shown that each of these hypotheses has a viable basis, they have only examined situations in which males have preferential access to food whereby females are required to obtain the food from males. For example, studies on male chimpanzee food sharing take advantage of successful crop-raids and/or acquisitions of meat from hunting, situations that only leave females access to food controlled by male food possessors. This begs the question how and with whom might a female chimpanzee in sole possession of a high-quality food item choose to share? In two large captive groups of chimpanzees, we examined each of the hypotheses with female food possessors of a high-quality food item and compared these data to a previous study examining food transfers from male chimpanzees. Our results show that alpha females shared significantly more with closely affiliated females displaying perseverance, while kinship and dominance rank had no effect. This positive interaction between long-term affiliation and perseverance shows that individuals with whom the female possessor was significantly affiliated received more food while persevering more than those with neutral or avoidant relationships towards her. Furthermore, females with avoidant relationships persevered far less than others, suggesting that this strategy is not equally available to all individuals. In comparison to the mixed-sex trials, females chose to co-feed with other females more than was observed when the alpha male was sharing food. This research indicates that male and female chimpanzees (as possessors of a desired food item) share food in ways influenced by different factors and strategies.