Rodrigo A. Medellín

Limits to the use of threatened species lists

Threatened species lists are designed primarily to provide an easily understood qualitative estimate of risk of extinction. Although these estimates of risk can be accurate, the lists have inevitably become linked to several decision-making processes. There are four ways in which such lists are commonly used: to set priorities for resource allocation for species recovery; to inform reserve system design; to constrain development and exploitation; and to report on the state of the environment. The lists were not designed for any one of these purposes, and consequently perform some of them poorly. We discuss why, if and how they should be used to achieve these purposes.

ASSESSING CONSERVATION PRIORITIES IN MEGADIVERSE MEXICO: MAMMALIAN DIVERSITY, ENDEMICITY, AND ENDANGERMENT

The identification of areas of high priority for conservation is becoming a major endeavor for conservation biologists. Regions of high species richness and high concentrations of endemic and endangered species have been considered a priority for conservation. In this paper we use information about the species richness, composition, and distribution of mammals from Mexico for selecting priority areas for conservation. All species of terrestrial mammals were characterized by geographic range size, body mass, and conservation status, and their distributions were overlaid on a 2° × 2° grid to detect areas of high concentrations of species richness, endemicity, and endangered species. We focused our analyses at both species and biogeographic levels. At the species level we examined differences among endangered, endemic, and non-endemic species in ecological characteristics correlated with vulnerability to extinction. There were significant differences between endangered and non-endangered species, and between endemic and non-endemic mammals in body size and geographic range size. At the biogeographic level simple correlation analyses were carried out to determine the relation between latitude, total species richness, number of endemic species, and number of endangered species. We found a very low correspondence among areas of high diversity, high endemicity, or high number of endangered species. The distribution of many species with restricted geographic ranges, including endemic and non-endemic species, did not coincide with areas of high species richness, endemicity, or endangerment. We suggest a conservation strategy that gives priority to areas of high concentration of endangered species and of non-endangered species with restricted distributions. Among endangered species a higher priority should be given to endemic taxa vs. non-endemic species, and to restricted species over widespread taxa in these two groups.

Genetic variation and migration in the Mexican free‐tailed bat (Tadarida brasiliensis mexicana)

Incomplete lineage sorting can genetically link populations long after they have diverged, and will exert a more powerful influence on larger populations. The effects of this stochastic process can easily be confounded with those of gene flow, potentially leading to inaccurate estimates of dispersal capabilities or erroneous designation of evolutionarily significant units (ESUs). We have used phylogenetic, population genetic, and coalescent methods to examine genetic structuring in large populations of a widely dispersing bat species and to test hypotheses concerning the influences of coalescent stochasticity vs. gene flow. The Mexican free‐tailed bat, Tadarida brasiliensis mexicana, exhibits variation in both migratory tendency and route over its range. Observations of the species’ migratory behaviour have led to the description of behaviourally and geographically defined migratory groups, with the prediction that these groups compose structured gene pools. Here, we used mtDNA sequence analyses coupled with existing information from allozyme, banding, and natural history studies to evaluate hypotheses regarding the relationship between migration and genetic structure. Analyses of molecular variance revealed no significant genetic structuring of behaviourally distinct migratory groups. Demographic analyses were consistent with population growth, although the timing of population expansion events differs between migratory and nonmigratory populations. Hypotheses concerning the role of gene flow vs. incomplete lineage sorting on these data are explored using coalescent simulations. Our study demonstrates the importance of accounting for coalescent stochasticity in formulating phylogeographical hypotheses, and indicates that analyses that do not take such processes into account can lead to false conclusions regarding a species’ phylogeographical history.

Coronaviruses in bats from Mexico

Bats are reservoirs for a wide range of human pathogens including Nipah, Hendra, rabies, Ebola, Marburg and severe acute respiratory syndrome coronavirus (CoV). The recent implication of a novel beta (β)-CoV as the cause of fatal respiratory disease in the Middle East emphasizes the importance of surveillance for CoVs that have potential to move from bats into the human population. In a screen of 606 bats from 42 different species in Campeche, Chiapas and Mexico City we identified 13 distinct CoVs. Nine were alpha (α)-CoVs; four were β-CoVs. Twelve were novel. Analyses of these viruses in the context of their hosts and ecological habitat indicated that host species is a strong selective driver in CoV evolution, even in allopatric populations separated by significant geographical distance; and that a single species/genus of bat can contain multiple CoVs. A β-CoV with 96.5 % amino acid identity to the β-CoV associated with human disease in the Middle East was found in a Nyctinomops laticaudatus bat, suggesting that efforts to identify the viral reservoir should include surveillance of the bat families Molossidae/Vespertilionidae, or the closely related Nycteridae/Emballonuridae. While it is important to investigate unknown viral diversity in bats, it is also important to remember that the majority of viruses they carry will not pose any clinical risk, and bats should not be stigmatized ubiquitously as significant threats to public health.

Moving across the border: modeling migratory bat populations

The migration of animals across long distances and between multiple habitats presents a major challenge for conservation. For the migratory Mexican free-tailed bat (Tadarida brasiliensis mexicana), these challenges include identifying and protecting migratory routes and critical roosts in two countries, the United States and Mexico. Knowledge and conservation of bat migratory routes is critical in the face of increasing threats from climate change and wind turbines that might decrease migratory survival. We employ a new modeling approach for bat migration, network modeling, to simulate migratory routes between winter habitat in southern Mexico and summer breeding habitat in northern Mexico and the southwestern United States. We use the model to identify key migratory routes and the roosts of greatest conservation value to the overall population. We measure roost importance by the degree to which the overall bat population declined when the roost was removed from the model. The major migratory routes—those with the greatest number of migrants—were between winter habitat in southern Mexico and summer breeding roosts in Texas and the northern Mexican states of Sonora and Nuevo Leon. The summer breeding roosts in Texas, Sonora, and Nuevo Leon were the most important for maintaining population numbers and network structure - these are also the largest roosts. This modeling approach contributes to conservation efforts by identifying the most influential areas for bat populations, and can be used to as a tool to improve our understanding of bat migration for other species. We anticipate this approach will help direct coordination of habitat protection across borders.

BRAZILIAN FREE‐TAILED BATS AS INSECT PEST REGULATORS IN TRANSGENIC AND CONVENTIONAL COTTON CROPS

During the past 12000 years agricultural systems have transitioned from natural habitats to conventional agricultural regions and recently to large areas of genetically engineered (GE) croplands. This GE revolution occurred for cotton in a span of slightly more than a decade during which a switch occurred in major cotton production areas from growing 100% conventional cotton to an environment in which 95% transgenics are grown. Ecological interactions between GE targeted insects and other insectivorous insects have been investigated. However, the relationships between ecological functions (such as herbivory and ecosystem transport) and agronomic benefits of avian or mammalian insectivores in the transgenic environment generally remain unclear, although the importance of some agricultural pest management services provided by insectivorous species such as the Brazilian free-tailed bat, Tadarida brasiliensis, have been recognized. We developed a dynamic model to predict regional-scale ecological functions in agricultural food webs by using the indicators of insect pest herbivory measured by cotton boll damage and insect emigration from cotton. In the south-central Texas Winter Garden agricultural region we find that the process of insectivory by bats has a considerable impact on both the ecology and valuation of harvest in Bacillus thuringiensis (Bt) transgenic and nontransgenic cotton crops. Predation on agricultural pests by insectivorous bats may enhance the economic value of agricultural systems by reducing the frequency of required spraying and delaying the ultimate need for new pesticides. In the Winter Garden region, the presence of large numbers of insectivorous bats yields a regional summer dispersion of adult pest insects from Bt cotton that is considerably reduced from the moth emigration when bats are absent in either transgenic or non-transgenic crops. This regional decrease of pest numbers impacts insect herbivory on a transcontinental scale. With a few exceptions, we find that the agronomics of both Bt and conventional cotton production is more profitable when large numbers of insectivorous bats are present.

Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies

The members of the Phyllostomidae, the New-World leaf-nosed family of bats, show a remarkable evolutionary diversification of dietary strategies including insectivory, as the ancestral trait, followed by appearance of carnivory and plant-based diets such as nectarivory and frugivory. Here we explore the microbiome composition of different feeding specialists: insectivore Macrotus waterhousii, sanguivore Desmodus rotundus, nectarivores Leptonycteris yerbabuenae and Glossophaga soricina, and frugivores Carollia perspicillata and Artibeus jamaicensis. The V4 region of the 16S rRNA gene from three intestinal regions of three individuals per species was amplified and community composition and structure was analyzed with α and β diversity metrics. Bats with plant-based diets had low diversity microbiomes, whereas the sanguivore D. rotundus and insectivore M. waterhousii had the most diverse microbiomes. There were no significant differences in microbiome composition between different intestine regions within each individual. Plant-based feeders showed less specificity in their microbiome compositions, whereas animal-based specialists, although more diverse overall, showed a more clustered arrangement of their intestinal bacterial components. The main characteristics defining microbiome composition in phyllostomids were species and feeding strategy. This study shows how differences in feeding strategies contributed to the development of different intestinal microbiomes in Phyllostomidae.

The Species–Area Relationship in Bat Assemblages of Tropical Caves

Abstract We tested for a relationship between number of bat species and surface area of 20 caves in central Mexico and investigated the role of the habitat diversity model as an explanation for this relationship. There was a significant positive correlation between the logarithm of species richness and the logarithm of cave surface area, evidence of a species–area relationship. Our data suggest that roost site diversity, as indicated by spatial variation in relative humidity and presence of avons (conical depressions in cave ceilings) is a cause of the species–area relationship.

POPULATION AND COMMUNITY ECOLOGY OF SMALL RODENTS IN MONTANE FOREST OF WESTERN MEXICO

Abstract This study reports results of a 14-month live-trap study of small-rodent communities in 2 habitats, cloud forest and disturbed areas, at Las Joyas Scientific Station of the Sierra de Manantlán Biosphere Reserve, western Mexico. Seven taxa of 2 families (Muridae, Heteromyidae) of small rodents were captured (Hodomys alleni, Liomys pictus, Oryzomys couesi, Peromyscus aztecus, Reithrodontomys fulvescens, R. sumichrasti, and Sigmodon alleni). Information about age structure, population dynamics, biomass, and reproduction were obtained with mark–recapture techniques for the most abundant species (P. aztecus and R. fulvescens) in both habitats. These species comprised 80.3% of the 707 captures in the cloud forest (P. aztecus, 51.2%; R. fulvescens, 29.1%), whereas, in the disturbed areas, R. fulvescens represented 81.7% of the 916 captures. Species varied in population density, relative abundance, and timing of reproduction, which was seasonal. Reproductive activity for P. aztecus peaked in the middle of the wet season (September 1995) in the cloud forest and in the wet season and middle of the dry-cold season (January 1996) in the disturbed areas. R. fulvescens showed reproductive activity in the wet season (July–October 1995) in both habitats. Density fluctuated annually for P. aztecus in both habitats, with a peak in January and February 1996; R. fulvescens showed the same patterns of density in both habitats with the highest values at the end of the wet season.

Adult Vampire Bats Produce Contact Calls When Isolated: Acoustic Variation by Species, Population, Colony, and Individual

Background Bat pups produce individually distinct isolation calls to facilitate maternal recognition. Increasing evidence suggests that, in group-living bat species, adults often use similar calls to maintain contact. We investigated if isolated adults from all three species of the highly cooperative vampire bats (Phyllostomidae: Desmodontinae) would produce vocally distinct contact calls when physically isolated. Methods/Principal Findings We assessed variation in contact calls recorded from isolated captive and wild-caught adult common vampire bats (Desmodus rotundus), white-winged vampire bats (Diaemus youngi) and hairy-legged vampire bats (Diphylla ecaudata). We compared species-typical contact call structure, and used information theory and permuted discriminate function analyses to examine call structure variation, and to determine if the individuality of contact calls is encoded by different call features across species and populations. We found that isolated adult vampire bats produce contact calls that vary by species, population, colony, and individual. However, much variation occurred within a single context and individual. We estimated signature information for captive Diaemus (same colony), captive Desmodus (same colony), and wild Desmodus (different colonies) at 3.21, 3.26, and 3.88 bits, respectively. Contact calls from a captive colony of Desmodus were less individually distinct than calls from wild-caught Desmodus from different colonies. Both the degree of individuality and parameters encoding individuality differed between the bats from a single captive colony and the wild-caught individuals from different groups. This result is consistent with, but not sufficient evidence of, vocal convergence in groups. Conclusion Our results show that adult vampire bats of all three species produce highly variable contact calls when isolated. Contact calls contain sufficient information for vocal discrimination, but also possess more intra-individual variation than is required for the sole purpose of identifying individuals.