Correction: Beyond words: From jaguar population trends to conservation and public policy in Mexico.

[This corrects the article DOI: 10.1371/journal.pone.0255555.].

Don't bury Mexico's biodiversity capacity.

In a world where biodiversity is on the line on many fronts-from armed conflict to pandemics to climate change-defending institutions that have effectively managed it is paramount. In the global effort to protect biodiversity, Mexico has been at the forefront. In particular, for more than 30 years, Mexico's National Commission for the Knowledge and Use of Biodiversity (CONABIO) has promoted research, compiled information on the biodiversity of Mexico and elsewhere, and connected academia, government, and society to guide decision-making. Unfortunately, the demise of CONABIO, which began in 2018 under the current administration, may be fully realized soon. Last month, the Mexican government announced its intent to reduce CONABIO from a multi-ministry federal government agency to a branch within the environment ministry. This will strip CONABIO of its independent voice, credibility, and influence on national and international policy. As this decision is open for public comment, it is important for the scientific community to speak out strongly against this change.

Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats.

Africa experiences frequent emerging disease outbreaks among humans, with bats often proposed as zoonotic pathogen hosts. We comprehensively reviewed virus-bat findings from papers published between 1978 and 2020 to evaluate the evidence that African bats are reservoir and/or bridging hosts for viruses that cause human disease. We present data from 162 papers (of 1322) with original findings on (1) numbers and species of bats sampled across bat families and the continent, (2) how bats were selected for study inclusion, (3) if bats were terminally sampled, (4) what types of ecological data, if any, were recorded and (5) which viruses were detected and with what methodology. We propose a scheme for evaluating presumed virus-host relationships by evidence type and quality, using the contrasting available evidence for Orthoebolavirus versus Orthomarburgvirus as an example. We review the wording in abstracts and discussions of all 162 papers, identifying key framing terms, how these refer to findings, and how they might contribute to people's beliefs about bats. We discuss the impact of scientific research communication on public perception and emphasize the need for strategies that minimize human-bat conflict and support bat conservation. Finally, we make recommendations for best practices that will improve virological study metadata.

Historical, temporal, and geographic dynamism of the interaction between Agave and Leptonycteris nectar-feeding bats.

PREMISE: The interaction between ecological and evolutionary processes has been recognized as an important factor shaping the evolutionary history of species. Some authors have proposed different ecological and evolutionary hypotheses concerning the relationships between plants and their pollinators; a special case is the interaction and suspected coevolution among Agave spp. and their main pollinators, the Leptonycteris bats. Agave spp. have, in general, a pollination syndrome compatible with chiropterophily including floral shape and size, nocturnal nectar production, and nectar quality and sugar concentration. Our goal was to analyze the interaction Agave-Leptonycteris and its dynamics during three different climate scenarios. METHODS: We modeled the Agave-Leptonycteris interaction in its spatial and temporal components during the Pleistocene using Ecological Niche Models (ENMs) and three climate scenarios: Current, Last Glacial Maximum (LGM), and Last InterGlacial (LIG). Furthermore, we analyzed the geographic correlation between 96 Agave spp. and two of the Mexican Tequila bats, genus Leptonycteris. RESULTS: We found that Leptonycteris spp. interact with different Agave spp. over their migratory routes. We propose an interaction refuge in Metztitlán and Tehuacán-Cuicatlán areas, where Agave- Leptonycteris interaction has probably remained active. During the nonmigratory season, both bat species consume nectar of almost the same Agave spp., suggesting the possibility of a diffuse coevolution among Agave and Leptonycteris bats. CONCLUSIONS: We propose that in the areas related to migratory bat movements, each bat species interacts with different Agave spp., whereas in the areas occupied by nonmigrant individuals, both bat species consume nectar of almost the same Agave taxa.

Our good neighbors: Understanding ecosystem services provided by insectivorous bats in Rwanda.

Bats are prodigious consumers of agricultural and forest pests, and are, therefore, a natural asset for agricultural productivity, suppressing populations of such pests. This study provides baseline information of diet of 143 bats belonging to eight insectivorous bat species from agricultural areas of Rwanda while evaluating the effectiveness of bats as pest suppressors. Using DNA metabarcoding to analyze bat fecal pellets, 85 different insect species were detected, with 60% (n = 65), 64% (n = 11) and 78% (n = 9) found to be agricultural pests from eastern, northern and western regions, respectively. Given the high percentages of agricultural pests detected, we submit that Rwandan insectivorous bats have the capacity for biocontrol of agricultural pests. Rwandan bat populations should be protected and promoted since they may foster higher crop yields and sustainable livelihoods.

Conservation genomics of Agave tequilana Weber var. azul: low genetic differentiation and heterozygote excess in the tequila agave from Jalisco, Mexico.

Background: Genetic diversity is fundamental for the survival of species. In particular, in a climate change scenario, it is crucial that populations maintain genetic diversity so they can adapt to novel environmental conditions. Genetic diversity in wild agaves is usually high, with low genetic differentiation among populations, in part maintained by the agave pollinators such as the nectarivorous bats. In cultivated agaves, patterns of genetic diversity vary according to the intensity of use, management, and domestication stage. In Agave tequilana Weber var. azul (A. tequilana thereafter), the plant used for tequila production, clonal propagation has been strongly encouraged. These practices may lead to a reduction in genetic diversity. Methods: We studied the diversity patterns with genome-wide SNPs, using restriction site associated DNA sequencing in cultivated samples of A. tequilana from three sites of Jalisco, Mexico. For one locality, seeds were collected and germinated in a greenhouse. We compared the genomic diversity, levels of inbreeding, genetic differentiation, and connectivity among studied sites and between adults and juvenile plants. Results: Agave tequilana presented a genomic diversity of HT = 0.12. The observed heterozygosity was higher than the expected heterozygosity. Adults were more heterozygous than juveniles. This could be a consequence of heterosis or hybrid vigor. We found a shallow genetic structure (average paired FST = 0.0044). In the analysis of recent gene flow, we estimated an average migration rate among the different populations of m = 0.25. In particular, we found a population that was the primary source of gene flow and had greater genomic diversity (HE and HO ), so we propose that this population should continue to be monitored as a potential genetic reservoir. Discussion: Our results may be the consequence of more traditional management in the studied specific region of Jalisco. Also, the exchange of seeds or propagules by producers and the existence of gene flow due to occasional sexual reproduction may play an important role in maintaining diversity in A. tequilana. For populations to resist pests, to continue evolving and reduce their risk of extinction under a climate change scenario, it is necessary to maintain genetic diversity. Under this premise we encourage to continue acting in conservation programs for this species and its pollinators.

Morphological Variation in the Wing Mite Periglischrus paracaligus (Acari: Spinturnicidae) Associated With Different Moving Strategies of the Host Leptonycteris yerbabuenae (Chiroptera: Phyllostomidae).

We evaluated the morphometric variation of wing mite Periglischrus paracaligus Herrin and Tipton, along with the distribution of their host Leptonycteris yerbabuenae Martinez and Villa, in Mexico. A total of 115 female and 96 male specimens of P. paracaligus were used to conduct linear and geometric morphometric analyses. We assessed the influence of the geographic distribution of the migratory and nonmigratory populations of its bat host species on changes in size and shape on these parasites. Both analyses revealed high intraspecific variation in P. paracaligus, but subtle geographic differentiation. None of the approaches used identified a consistent pattern that separates unambiguously migratory from nonmigratory populations. Females presented more phenotypic variation than males and UPGMA analyses showed southern and northern colonies grouped in two distinct clades. Males on the other hand showed randomly grouped colonies with no geographic concordance. Interestingly, the most differentiated colony was the north Pacific colony of Jalisco. For both, males and females, isolation by distance (IBD) was not observed. We discuss these results as a possible scenario of contact between migratory populations located in northern Mexico with nonmigratory populations in other localities in central and southern Mexico conforming to a panmictic population along with their distribution range.

Traveler Mites: Population Genetic Structure of the Wing Mites Periglischrus paracaligus (Acari: Mesostigmata: Spinturnicidae).

Wing mites of the genus Periglischrus are ectoparasites exclusively associated with phyllostomid bats. These mites show high host specificity and have been studied to understand the evolutionary history of their bat hosts mainly by using a morphological variation. Through a phylogeographic approach, we analyzed the genetic diversity and population genetic structure of the ectoparasite Periglischrus paracaligus Herrin and Tipton which parasitizes Leptonycteris yerbabuenae Martínez and Villa (lesser long-nosed bat) in Mexico. By the implementation of a multilocus approach, we found that P. paracaligus populations were diverse for haplotype diversity, and had values ranging from 0.5 to 1. No genetic structuring in the P. paracaligus parasites was observed along with the distribution of the host, L. yerbabuenae, in Mexico, nor when populations or regions were compared, but our results revealed a process of historical demographic expansion in all the analyzed markers. We discuss possible scenarios that could explain the lack of population structure in the light of the data analyzed for the parasites and the biology of L. yerbabuenae, such as the interplay between parasite and host traits being responsible for the genetic make-up of parasite populations. We also inferred its phylogenetic position among wing mites parasitizing the two other species of Leptonycteris bats. Long-nosed bats' monophyly helps to explain the observed presence of distinctive clades in the wing mite's phylogeny in specific association with each long-nosed bat host species.

Uses, Knowledge and Extinction Risk Faced by Agave Species in Mexico.

We compiled an updated database of all Agave species found in Mexico and analyzed it with specific criteria according to their biological parameters to evaluate the conservation and knowledge status of each species. Analyzing the present status of all Agave species not only provides crucial information for each species, but also helps determine which ones require special protection, especially those which are heavily used or cultivated for the production of distilled beverages. We conducted an extensive literature review search and compiled the conservation status of each species using mainstream criteria by IUCN. The information gaps in the database indicate a lack of knowledge and research regarding specific Agave species and it validates the need to conduct more studies on this genus. In total, 168 Agave species were included in our study, from which 89 are in the subgenus Agave and 79 in the subgenus Littaea. Agave lurida and A. nizandensis, in the subgenus Agave and Littaea, respectively, are severely endangered, due to their endemism, lack of knowledge about pollinators and floral visitors, and their endangered status according to the IUCN Red List. Some species are at risk due to the loss of genetic diversity resulting from production practices (i.e., Agave tequilana), and others because of excessive and unchecked overharvesting of wild plants, such as A. guadalajarana, A. victoriae-reginae, A. kristenii, and others. Given the huge economic and ecological importance of plants in the genus Agave, our review will be a milestone to ensure their future and continued provision of ecosystem services for humans, as well as encouraging further research in Agave species in an effort to enhance awareness of their conservation needs and sustainable use, and the implementation of eco-friendly practices in the species management.

A Faithful Gut: Core Features of Gastrointestinal Microbiota of Long-Distance Migratory Bats Remain Stable despite Dietary Shifts Driving Differences in Specific Bacterial Taxa.

Migratory animals live in a world of constant change. Animals undergo many physiological changes preparing themselves for the migration. Although this field has been studied extensively over the last decades, we know relatively little about the seasonal changes that occur in the microbial communities that these animals carry in their guts. Here, we assessed the V4 region of the 16S rRNA high-throughput sequencing data as a proxy to estimate microbiome diversity of tequila bats from fecal pellets and evaluate how the natural process of migration shapes the microbiome composition and diversity. We collected samples from individual bats at two localities in the dry forest biome (Chamela and Coquimatlán) and one site at the endpoint of the migration in the Sonoran Desert (Pinacate). We found that the gut microbiome of the tequila bats is dominated largely by Firmicutes and Proteobacteria. Our data also provide insights on how microbiome diversity shifts at the same site in consecutive years. Our study has demonstrated that both locality and year-to-year variation contribute to shaping the composition, overall diversity, and "uniqueness" of the gut microbiome of migratory nectar-feeding female bats, with localities from the dry forest biome looking more like each other compared to those from the desert biome. In terms of beta diversity, our data show a stratified effect in which the samples' locality was the strongest factor influencing the gut microbiome but with significant variation between consecutive years at the same locality. IMPORTANCE Migratory animals live in a world of constant change. The whole-body ecosystem needs a strong adapting capacity to thrive despite the changes. Our study used next-generation sequencing to determine how gut microbial change along the migratory path of the nectar-feeding tequila bats. The study of the gut microbiome is a great tool that can provide important insights that are relevant not just for management and conservation but also an initial investigation of the extent of the adaptation and preparedness of the individual animals, with respect not just to their current environment but also to all the environments involved in their yearly cycle.

Discordance in maternal and paternal genetic markers in lesser long-nosed bat Leptonycteris yerbabuenae, a migratory bat: recent expansion to the North and male phylopatry.

Leptonycteris yerbabuenae, the lesser long-nosed bat is an abundant migratory nectar-feeding bat found in most of Mexico, and in some areas of northern Central America and small sections of southwestern USA. We analyzed the distribution of the maternal and paternal lineages of this species with phylogeographic methods based on two mitochondrial markers, Cyt-b and D-loop, and a marker located in the Y chromosome, DBY. We obtained tissue samples from 220 individuals from 23 localities. Levels of genetic diversity (haplotype diversity, Hd ) were high (Cyt-b = 0.757; D-loop = 0.8082; DBY = 0.9137). No clear patterns of population genetic structure were found for mitochondrial markers, while male genetic differentiation suggested the presence of two lineages: one from Mexican Pacific coast states and another from central-southern Mexico; in accordance to strong male philopatry and higher female migration. We used genealogical reconstructions based on Bayesian tools to calculate divergence times, and to test coalescent models to explain changes in L. yerbabuenae historical demography. Our results show that recent demographic changes were consistent with global climatic changes (∼130,000 kyr ago for Cyt-b and ∼160,000 kyr for D-loop) and divergence times dated from molecular genealogies exhibited older divergence times, Cyt-b (4.03 mya), D-loop (10.26 mya) and DBY (12.23 mya). Accordingly, the female lineage underwent demographic expansion associated to Pleistocene climate change, whereas the male lineage remained constant.

Beyond words: From jaguar population trends to conservation and public policy in Mexico.

The jaguar (Panthera onca) is one of the most threatened carnivores in the Americas. Despite a long history of research on this charismatic species, to date there have been few systematic efforts to assess its population size and status in most countries across its distribution range. We present here the results of the two National Jaguar Surveys for Mexico, the first national censuses in any country within the species distribution. We estimated jaguar densities from field data collected at 13 localities in 2008-2010 (2010 hereafter) and 11 localities in 2016-2018 (2018 hereafter). We used the 2010 census results as the basis to develop a National Jaguar Conservation Strategy that identified critical issues for jaguar conservation in Mexico. We worked with the Mexican government to implement the conservation strategy and then evaluated its effectivity. To compare the 2010 and 2018 results, we estimated the amount of jaguar-suitable habitat in the entire country based on an ecological niche model for both periods. Suitable jaguar habitat covered ~267,063 km2 (13.9% of the country's territory) in 2010 and ~ 288,890 km2 (~14.8% of the country's territory) in 2018. Using the most conservative density values for each priority region, we estimated jaguar densities for both the high and low suitable habitats. The total jaguar population was estimated in ~4,000 individuals for 2010 census and ~4,800 for the 2018 census. The Yucatan Peninsula was the region with the largest population, around 2000 jaguars, in both censuses. Our promising results indicate that the actions we proposed in the National Jaguar Conservation Strategy, some of which have been implemented working together with the Federal Government, other NGO's, and land owners, are improving jaguar conservation in Mexico. The continuation of surveys and monitoring programs of the jaguar populations in Mexico will provide accurate information to design and implement effective, science-based conservation measures to try to ensure that robust jaguar populations remain a permanent fixture of Mexico's natural heritage.

Setting the Terms for Zoonotic Diseases: Effective Communication for Research, Conservation, and Public Policy.

Many of the world's most pressing issues, such as the emergence of zoonotic diseases, can only be addressed through interdisciplinary research. However, the findings of interdisciplinary research are susceptible to miscommunication among both professional and non-professional audiences due to differences in training, language, experience, and understanding. Such miscommunication contributes to the misunderstanding of key concepts or processes and hinders the development of effective research agendas and public policy. These misunderstandings can also provoke unnecessary fear in the public and have devastating effects for wildlife conservation. For example, inaccurate communication and subsequent misunderstanding of the potential associations between certain bats and zoonoses has led to persecution of diverse bats worldwide and even government calls to cull them. Here, we identify four types of miscommunication driven by the use of terminology regarding bats and the emergence of zoonotic diseases that we have categorized based on their root causes: (1) incorrect or overly broad use of terms; (2) terms that have unstable usage within a discipline, or different usages among disciplines; (3) terms that are used correctly but spark incorrect inferences about biological processes or significance in the audience; (4) incorrect inference drawn from the evidence presented. We illustrate each type of miscommunication with commonly misused or misinterpreted terms, providing a definition, caveats and common misconceptions, and suggest alternatives as appropriate. While we focus on terms specific to bats and disease ecology, we present a more general framework for addressing miscommunication that can be applied to other topics and disciplines to facilitate more effective research, problem-solving, and public policy.

Environmental and anthropogenic factors synergistically affect space use of jaguars.

Large terrestrial carnivores have undergone some of the largest population declines and range reductions of any species, which is of concern as they can have large effects on ecosystem dynamics and function.1-4 The jaguar (Panthera onca) is the apex predator throughout the majority of the Neotropics; however, its distribution has been reduced by >50% and it survives in increasingly isolated populations.5 Consequently, the range-wide management of the jaguar depends upon maintaining core populations connected through multi-national, transboundary cooperation, which requires understanding the movement ecology and space use of jaguars throughout their range.6-8 Using GPS telemetry data for 111 jaguars from 13 ecoregions within the four biomes that constitute the majority of jaguar habitat, we examined the landscape-level environmental and anthropogenic factors related to jaguar home range size and movement parameters. Home range size decreased with increasing net productivity and forest cover and increased with increasing road density. Speed decreased with increasing forest cover with no sexual differences, while males had more directional movements, but tortuosity in movements was not related to any landscape factors. We demonstrated a synergistic relationship between landscape-scale environmental and anthropogenic factors and jaguars' spatial needs, which has applications to the conservation strategy for the species throughout the Neotropics. Using large-scale collaboration, we overcame limitations from small sample sizes typical in large carnivore research to provide a mechanism to evaluate habitat quality for jaguars and an inferential modeling framework adaptable to the conservation of other large terrestrial carnivores.

DNA methylation predicts age and provides insight into exceptional longevity of bats.

Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.

Cuba in Mexico: first record of Phyllops falcatus (Gray, 1839) (Chiroptera, Phyllostomidae) for Mexico and other new records of bats from Cozumel, Quintana Roo.

The first record of Phyllops falcatus (Gray, 1839) in Mexico is documented from the island of Cozumel, Quintana Roo. This species is present in the Antilles, distributed in all the Cuban archipelago, Cayman Islands, and Hispaniola. It is likely that a hurricane moved these bats from Cuba to Cozumel. The Cozumel record extends the distribution more than 200 km west. Two new records from Cozumel of the bats Lasiurus ega and Molossus alvarezi are also provided.