Rapid taxonomic categorization of short, abundant virus sequences for ecological analyses.

Public health concerns about recent viral epidemics have motivated researchers to seek novel ways to understand pathogen infection in native, wildlife hosts. With its deep history of tools and perspectives for understanding the abundance and distribution of organisms, ecology can shed new light on viral infection dynamics. However, datasets allowing deep explorations of viral communities from an ecological perspective are lacking. We sampled 1086 bats from two, adjacent Puerto Rican caves and tested them for infection by herpesviruses, resulting in 3131 short, viral sequences. Using percent identity of nucleotides and a machine learning algorithm (affinity propagation), we categorized herpesviruses into 43 operational taxonomic units (OTUs) to be used in place of species in subsequent ecological analyses. Herpesvirus metacommunities demonstrated long-tailed rank frequency distributions at all analyzed levels of host organization (i.e., individual, population, and community). Although 13 herpesvirus OTUs were detected in more than one host species, OTUs generally exhibited host specificity by infecting a single core host species at a significantly higher prevalence than in all satellite species combined. We describe the natural history of herpesvirus metacommunities in Puerto Rican bats and suggest that viruses follow the general law that communities comprise few common and many rare species. To guide future efforts in the field of viral ecology, hypotheses are presented regarding mechanisms that contribute to these patterns.

Reproductive phenologies of phyllostomid bat populations and ensembles from lowland Amazonia.

Natural selection should favor individuals that synchronize energy-demanding aspects of reproductive activity with periods of high resource abundance and predictability, leading to seasonal patterns of reproduction at the population level. Nonetheless, few studies-especially those on bats in the Neotropics-have used rigorous quantitative criteria to distinguish among phenological patterns for different populations from the same habitat or for the same species in different habitats. To explore such issues, we quantified annual patterns of reproduction in male and in female bats from lowland Amazonia (environs of Iquitos, Peru), and did so at the level of populations and ensembles. Five species exhibited unimodal patterns including Artibeus obscurus, A. planirostris, Carollia benkeithi, Phyllostomus hastatus, and Rhinophylla pumilio. Two species (A. lituratus and Glossophaga soricina) evinced bimodal patterns with reproductive peaks separated by patterns of inactivity, whereas four species (C. brevicauda, C. perspicillata, Sturnira lilium, and S. tildae) evinced a bimodal pattern in which peaks in activity occur in tandem, with the first peak generally markedly higher than the second peak. Frugivore, gleaning animalivore, and nectarivore ensembles exhibited bimodal, unimodal, and bimodal reproductive phenologies, respectively. Nonetheless, interannual variation in phenology (i.e., the monthly timing of peaks within a season rather than the number of peaks per year) characterized four (A. obscurus, C. brevicauda, C. perspicillata, and S. lilium) of the eight species and each of the three ensembles (frugivores, gleaning animalivores, and nectarivores) with adequate sampling. Regardless of interspecific variation in strategies, the phenology of reproduction enhances the likelihood that parturition and recruitment of young into the population occurs during the wet season, the period of likely highest resource abundance. Based on a comparison of our results with those from other well-studied bat populations, four species did not exhibit geographic variation in reproductive phenologies (A. obscurus, G. soricina, C. brevicauda, and R. pumilio), whereas three species evinced such geographic variation (A. lituratus, A. planirostris, and C. perspicillata). Climate change will likely alter the seasons and extents of propitious times for reproductive activities, as well as the reliability of proximate cues for initiating reproduction, compromising current reproductive strategies and leading to altered phenological patterns of reproduction or reproductive success, possibly resulting in local extinction of some species.

La selección natural debería favorecer a individuos que sincronicen aspectos de alta demanda de energía en su actividad reproductiva con períodos de alta abundancia y previsibilidad de recursos, lo que conduciría a patrones estacionales de reproducción a nivel poblacional. No obstante, pocos estudios, especialmente estudios sobre murciélagos en el Neotrópico, han utilizado criterios cuantitativos rigurosos para distinguir entre patrones fenológicos ya sea para diferentes poblaciones dentro del mismo hábitat o para la misma especie en diferentes hábitats. Para explorar este tema, cuantificamos los patrones anuales de reproducción de murciélagos machos (porcentaje de la población con testículos escrotales) y hembras (porcentaje de la población embarazada o lactante) en regiones bajas de la Amazonía (alrededores de Iquitos, Perú) a nivel de poblaciones y de ensamblajes. Cinco especies exhibieron patrones unimodales, incluidos Artibeus obscurus, Artibeus planirostris, Carollia benkeithi, Phyllostomus hastatus, y Rhinophylla pumilio. Dos especies (Artibeus lituratus y Glossophaga soricina) mostraron patrones bimodales, con picos reproductivos separados por patrones de inactividad, mientras que cuatro especies (Carollia brevicauda, Carollia perspicillata, Sturnira lilium, y Sturnira tildae) mostraron un patrón bimodal en el que los picos de actividad ocurren en tándem, con un primer pico considerablemente más alto que el segundo. Los grupos de frugívoros, animalívoros y nectarívoros exhibieron fenologías reproductivas bimodales, unimodales y bimodales respectivamente. No obstante, la variación interanual en la fenología (es decir, el mes dentro de una temporada en que ocurren los picos en lugar del número de picos por año) caracterizó a cuatro (A. obscurus, C. brevicauda, C. perspicillata y S. lilium) de las ocho especies y cada uno de los tres ensamblajes (frugívoros, animalívoros y nectarívoros) con un tamaño de muestra adecuado. Independientemente de la variación en las estrategias, la fenología en la reproducción aumenta la probabilidad de que el parto y el reclutamiento de crías en la población ocurran en la estación húmeda, el período de mayor abundancia de recursos. Cuando comparamos nuestros resultados con los de otras poblaciones de murciélagos mejor estudiadas, cuatro especies no mostraron variación geográfica en sus estrategias reproductivas (A. obscurus, G. soricina, C. brevicauda y R. pumilio), mientras que tres especies si mostraron esta variación geográfica (A. lituratus, A. planirostris y C. perspicillata). Es probable que el cambio climático altere las estaciones y la duración de los periodos propicios para el desarrollo de actividades reproductivas de alta demanda de energía, así como la regularidad de las señales activantes para iniciar la actividad reproductiva, comprometiendo las estrategias reproductivas actuales y conllevando a patrones fenológicos de reproducción alterados, lo que para algunas especies podría resultar en extinciones locales.

Long-term spatiotemporal variation in density of a tropical folivore: responses to a complex disturbance regime.

The Anthropocene is a time of unprecedented and accelerating rates of environmental change that includes press (e.g., climate change) and pulse disturbances (e.g., cyclonic storms, land use change) that interact to affect spatiotemporal dynamics in the density, distribution, and biodiversity of organisms. We leverage three decades of spatially explicit data on the density of a tropical folivore (Lamponius portoricensis [Insecta, Phasmida]) in a hurricane-mediated ecosystem (montane rainforest of Puerto Rico), along with associated environmental attributes, to disentangle the effects of interacting disturbances at multiple spatial scales. Spatiotemporal variation in density at a small spatial scale is affected by disturbance-related characteristics (hurricane severity, time after most recent major hurricane, ambient temperature, and understory temperature), legacies of previous land use, and understory habitat structure. Nonetheless, only a small proportion of spatiotemporal variation in density was related to those characteristics. In contrast, the majority of interannual variation in mean density at a larger scale was related to disturbance characteristics and understory habitat structure. These factors combine to affect a weak and declining trend in the density of L. portoricensis over time. The low resistance of L. portoricensis to Hurricane Hugo, as compared to Hurricanes Georges and Maria, likely arose because a drought followed Hurricane Hugo. The disturbance regime of the region is predicted to include increases in ambient temperatures, frequency of high-intensity storms, and frequency of droughts. Such trends may combine to threaten the conservation status of L. portoricensis, and other species with which it shares similar life history characteristics.

From island biogeography to landscape and metacommunity ecology: A macroecological perspective of bat communities.

The equilibrium theory of island biogeography and its quantitative consideration of origination and extinction dynamics as they relate to island area and distance from source populations have evolved over time and enriched theory related to many disciplines in spatial ecology. Indeed, the island focus was catalytic to the emergence of landscape ecology and macroecology in the late 20th century. We integrate concepts and perspectives of island biogeography, landscape ecology, macroecology, and metacommunity ecology, and show how these disciplines have advanced the understanding of variation in abundance, biodiversity, and composition of bat communities. We leverage the well-studied bat fauna of the islands in the Caribbean to illustrate the complex interplay of ecological, biogeographical, and evolutionary processes in molding local biodiversity and system-wide structure. Thereafter, we highlight the role of habitat loss and fragmentation, which is increasing at an accelerating rate during the Anthropocene, on the structure of local bat communities and regional metacommunities across landscapes. Bat species richness increases with the amount of available habitat, often forming nested subsets along gradients of patch or island area. Similarly, the distance to and identity of sources of colonization influence the richness, composition, and metacommunity structure of islands and landscape networks.

Effects of Host Species Identity and Diet on the Biodiversity of the Microbiota in Puerto Rican Bats.

Microbiota perform vital functions for their mammalian hosts, making them potential drivers of host evolution. Understanding effects of environmental factors and host characteristics on the composition and biodiversity of the microbiota may provide novel insights into the origin and maintenance of these symbiotic relationships. Our goals were to (1) characterize biodiversity of oral and rectal microbiota in bats from Puerto Rico; and (2) determine the effects of geographic location and host characteristics on that biodiversity. We collected bats and their microbiota from three sites, and used four metrics (species richness, Shannon diversity, Camargo evenness, Berger-Parker dominance) to characterize biodiversity. We quantified the relative importance of site, host sex, host species-identity, and host foraging-guild on biodiversity of the microbiota. Microbe biodiversity was highly variable among conspecifics. Geographical location exhibited consistent effects, whereas host sex did not. Within each host guild, host species exhibited consistent differences in biodiversity of oral microbiota and of rectal microbiota. Oral microbe biodiversity was indistinguishable between guilds, whereas rectal microbe biodiversity was significantly greater in carnivores than in herbivores. The high intraspecific and spatial variation in microbe biodiversity necessitate a relatively large number of samples to statistically isolate the effects of environmental or host characteristics on the microbiota. Species-specific biodiversity of oral microbiota suggests these communities are structured by direct interactions with the host immune system via epithelial receptors. In contrast, the number of microbial taxa that a host gut supports may be driven by host diet-diversity or composition.

A canonical metacommunity structure over 3 decades: ecologically consistent but spatially dynamic patterns in a hurricane-prone montane forest.

The Anthropocene is a time of rapid change induced by human activities, including pulse and press disturbances that affect the species composition of local communities and connectivity among them, giving rise to spatiotemporal dynamics at multiple scales. We evaluate effects of global warming and repeated intense hurricanes on gastropod metacommunities in montane tropical rainforests of Puerto Rico for each of 28 consecutive years. Specifically, we quantified metacommunity structure each year; assessed effects of global warming, hurricane-induced disturbance, and secondary succession on interannual variation in metacommunity structure; and evaluated legacies of previous land use on metacommunity structure. Gastropods were sampled annually during a 28-year period characterized by disturbance and succession associated with 3 major hurricanes (Hurricanes Hugo, Georges, and Maria). For each year, we evaluated coherence (the extent to which the environmental distributions of species are uninterrupted along a common latent environmental gradient), species range turnover, and species range boundary clumping; and conducted co-occurrence analyses for each pair of species. We used generalized linear mixed-effects model to evaluate long-term responses of the metacommunity to aspects of global warming and disturbance. Metacommunity structure was remarkably stable, with consistent patterns of species co-occurrence. Disturbance, warming, and successional stage had little effect on metacommunity structure. Despite great temporal variation in environmental conditions, groups of species tracked their niche through space and time to maintain the same general structure. Consequently, metacommunity structure was highly resistant and resilient to multiple disturbances, even those that greatly altered forest structure.

Arthropods are not declining but are responsive to disturbance in the Luquillo Experimental Forest, Puerto Rico.

A number of recent studies have documented long-term declines in abundances of important arthropod groups, primarily in Europe and North America. These declines are generally attributed to habitat loss, but a recent study [B.C. Lister, A. Garcia, Proc. Natl. Acad. Sci. USA 115, E10397-E10406 (2018)] from the Luquillo Experimental Forest (LEF) in Puerto Rico attributed declines to global warming. We analyze arthropod data from the LEF to evaluate long-term trends within the context of hurricane-induced disturbance, secondary succession, and temporal variation in temperature. Our analyses demonstrate that responses to hurricane-induced disturbance and ensuing succession were the primary factors that affected total canopy arthropod abundances on host trees, as well as walkingstick abundance on understory shrubs. Ambient and understory temperatures played secondary roles for particular arthropod species, but populations were just as likely to increase as they were to decrease in abundance with increasing temperature. The LEF is a hurricane-mediated system, with major hurricanes effecting changes in temperature that are larger than those induced thus far by global climate change. To persist, arthropods in the LEF must contend with the considerable variation in abiotic conditions associated with repeated, large-scale, and increasingly frequent pulse disturbances. Consequently, they are likely to be well-adapted to the effects of climate change, at least over the short term. Total abundance of canopy arthropods after Hurricane Maria has risen to levels comparable to the peak after Hurricane Hugo. Although the abundances of some taxa have declined over the 29-y period, others have increased, reflecting species turnover in response to disturbance and secondary succession.

Functional volumes, niche packing and species richness: biogeographic legacies in the Congo Basin.

Understanding the determinants of species coexistence in complex and species-rich communities is a fundamental goal of ecology. Patterns of species coexistence depend on how biotic interactions and environmental filtering act over ecological and evolutionary time scales. Climatic fluctuations in lowland rainforests of the Congo Basin led to the number of vertebrate species being significantly lower in central compared with northern ecoregions of the Basin. We used null models to assess whether climatic variations affected the community assembly of shrews. A consistent limit to functional similarity of species was not related to species richness. Rather, species richness is constrained by environmental factors, and these constraints are stronger in the central lowland forests of the Congo Basin. By constraining species geographic distributions, historical effects of rainforest refugia arising from climatic fluctuations may affect contemporary species composition of local shrew communities. The Congo River represents a vicariance event that led to allopatric speciation of shrews and continues to represent a barrier to dispersal. Ultimately, the historical effects of this barrier have led to differences in the functional volume of shrew communities in northern and central ecoregions. We suggest that the analyses of community assembly can be used to identify Holocene refugia in the Congo Basin.

Phylogenetic supertree and functional trait database for all extant parrots.

We present a complete dataset from the literature on functional traits including morphological measurements, dietary information, foraging strategy, and foraging location for all 398 extant species of parrots. The morphological measurements include: mass, total length, wing chord, culmen length, tarsus length, and tail length. The diet data describe whether each species is known to consume particular food items (e.g. nectar, berries, and carrion), foraging strategy data describes how each species captures or accesses food, and foraging location data describe the habitat from which each species finds food (e.g. ground, canopy, and subcanopy). We also present a time-calibrated phylogenetic supertree that contains all 398 extant species as well as 15 extinct species (413 total species). These data are hosted on the Figshare data depository (https://figshare.com/s/6cdf8cf00793deab7ba6).

Checkerboard metacommunity structure: an incoherent concept.

Checkerboards have emerged as a metaphor to (1) describe mutually exclusive patterns of co-occurrence for ecologically similar species that are geographically interspersed (i.e., checkerboard distributions), and (2) characterize relationships among species distributions along gradients that involve entire metacommunities (i.e., checkerboard metacommunity structure). Critical differences exist in the conceptual foundations that characterize these patterns. Checkerboard distributions are characterized by mutual exclusion of geographically interspersed species, usually pairs of ecologically similar species for which competition prevents syntopy. In contrast, checkerboard metacommunity structures are more restrictive: groups of species must exhibit mutually exclusive distributions, and each of these groups must be spatially independent of all other groups. Consequently, in a checkerboard metacommunity, competition defines one relationship for each species (i.e., that with its mutually exclusive partner), whereas independence characterizes all other interspecific associations. Consequently, a structure designed to be consistent with this concept will conclude that the metacommunity has random rather than checkerboard structure. Indeed, empirical checkerboard metacommunities are quite rare (7 of 766 reported empirical structures), and likely arise because of poor characterization of species ranges due to detection errors (i.e., a preponderance of rare or hard-to-detect species), rather than from underlying ecological mechanisms. Importantly, no ecological mechanism has been identified that is consistent with the concept of negative coherence. Consequently, the evaluation of checkerboards should be restricted to small sets of ecologically similar species for which interspecific interactions may lead to mutual exclusion, and coherence should be used only to evaluate if species distributions are more coherent than expected by chance (i.e., one-tailed tests).

Guild-level responses of bats to habitat conversion in a lowland Amazonian rainforest: species composition and biodiversity.

Landscape modification represents one of the most severe threats to biodiversity from local to global scales. Conversion of forest to agricultural production generally results in patches of habitat that subdivide or isolate populations, alter the behavior of species, modify interspecific interactions, reduce biodiversity, and compromise ecosystem processes. Moreover, conversion may increase exposure of humans to zoonoses to which they would otherwise rarely be exposed. We evaluated the effects of forest conversion to agriculture, and its subsequent successional dynamics, on bat communities in a region of the Amazon that was predominantly closed-canopy rainforest. Based on a nonmanipulative experiment, we quantified differences in species composition, community structure, and taxonomic biodiversity among closed-canopy forest (bosque), agricultural lands (chacra), and secondary forest (purma) for two phyllostomid guilds (frugivores and gleaning animalivores) during the wet and dry seasons. Responses were complex and guild-specific. For frugivores, species composition (species abundance distributions) differed between all possible pairs of habitats in both wet and dry seasons. For gleaning animalivores, species composition differed between all possible pairs of habitats in the dry season, but no differences characterized the wet season. Ecological structure (rank abundance distributions) differed among habitats in guild-specific and season-specific manners. For frugivores, mean diversity, evenness, and dominance were greater in bosque than in purma; mean dominance was greater in bosque than in chacra, but local rarity was greater in chacra than in bosque, and no differences were manifest between purma and chacra. For gleaning animalivores, mean diversity and evenness were greater in bosque than in purma, but no differences were manifest between chacra and bosque, or between purma and chacra. Such results have important implications for management, conservation, and the epidemiology of zoonotic diseases. La actual modificación del paisaje, a escalas que van de lo local a lo global, es una de las amenazas más severas a la biodiversidad. De manera general, la conversión de bosques a áreas agrícolas produce parches de hábitat que subdividen o aíslan poblaciones, alteran la conducta de las especies, modifican las interacciones interespecíficas, reducen la biodiversidad y comprometen las funciones de los ecosistemas. Más aún, la transformación de estos ambientes puede incrementar la probabilidad de que las poblaciones humanas interactúen con zoonosis con las que de otra manera raramente entrarían en contacto. Evaluamos los efectos de la conversión de hábitat en comunidades de murciélagos en una región de Amazonia en la que la vegetación dominante es un bosque lluvioso de copas cerradas, y en la cual los efectos de la conversión a usos agrícolas sobre la biodiversidad, y la subsecuente dinámica sucesional, son aún poco comprendidos. Por medio de un experimento no-manipulativo, cuantificamos las diferencias en composición de especies, estructura de la comunidad y diversidad taxonómica entre bosque cerrado (bosque), áreas agrícolas (chacra) y bosque secundario (purma) para dos gremios tróficos de murciélagos filostómidos (frugívoros y forrajeadores de sustrato) durante dos temporadas (secas y lluvias). Las respuestas fueron complejas y diferentes para cada gremio. Para los frugívoros, la composición de especies (distribución de las abundancias) fue diferente para todos los posibles pares de hábitats tanto para secas como para lluvias. Para los forrajeadores de sustrato, la composición de especies difirió entre todos los posibles pares de hábitats en la temporada seca, pero no en la de lluvias. La estructura ecológica (distribuciones rango-abundancia) fue también específica para gremios y temporadas. Para los frugívoros, la diversidad promedio, equidad y dominancia fueron mayores en bosque que en purma; la dominancia promedio fue mayor en bosque que en chacra, pero la rareza local fue mayor en chacra que en bosque, y no se encontraron diferencias entre purma y chacra. Para los forrajeadores de sustrato, la diversidad promedio y la dominancia fueron mayores en bosque que en purma, pero no se detectaron diferencias entre chacra y bosque, o entre purma y chacra. Estos resultados tienen importantes implicaciones para el manejo, conservación y epidemiología de zoonosis.

Reconciling biodiversity and carbon stock conservation in an Afrotropical forest landscape.

Protecting aboveground carbon stocks in tropical forests is essential for mitigating global climate change and is assumed to simultaneously conserve biodiversity. Although the relationship between tree diversity and carbon stocks is generally positive, the relationship remains unclear for consumers or decomposers. We assessed this relationship for multiple trophic levels across the tree of life (10 organismal groups, 3 kingdoms) in lowland rainforests of the Congo Basin. Comparisons across regrowth and old-growth forests evinced the expected positive relationship for trees, but not for other organismal groups. Moreover, differences in species composition between forests increased with difference in carbon stock. These variable associations across the tree of life contradict the implicit assumption that maximum co-benefits to biodiversity are associated with conservation of forests with the highest carbon storage. Initiatives targeting climate change mitigation and biodiversity conservation should include both old-growth and regenerating forests to optimally benefit biodiversity and carbon storage.

The components of biodiversity, with a particular focus on phylogenetic information.

We present a framework for biodiversity metrics that organizes the growing panoply of metrics. Our framework distinguishes metrics based on the type of information-abundance, phylogeny, function-and two common properties-magnitude and variability. Our new metrics of phylogenetic diversity are based on a partition of the total branch lengths of a cladogram into the proportional share of each species, including: a measure of divergence which standardizes the amount of evolutionary divergence by species richness and time depth of the cladogram; a measure of regularity which is maximal when the tree is perfectly symmetrical so that all species have the same proportional branch lengths; a measure that combines information on the magnitude and variability of abundance with phylogenetic variability, and a measure of phylogenetically weighted effective mean abundance; and indicate how those metrics can be decomposed into α and ß components. We illustrate the utility of these new metrics using empirical data on the bat fauna of Manu, Peru. Divergence was greatest in lowland rainforest and at the transition between cloud and elfin forests, and least in upper elfin forests and in cloud forests. In contrast, regularity was greatest in lowland rainforest, dipping to its smallest values in mid-elevation cloud forests, and then increasing in high elevation elfin forests. These patterns indicate that the first species to drop out with increasing elevation are ones that are closely related to other species in the metacommunity. Measures of the effective number of phylogenetically independent or distinct species decreased very rapidly with elevation, and ß-diversity was larger. In contrast, a comparison of feeding guilds shows a different effect of phylogenetic patterning. Along the elevational gradient, each guild generally loses some species from each clade-rather than entire clades-explaining the maintenance of functional diversity as phylogenetic diversity decreases.

Environmental and spatial drivers of taxonomic, functional, and phylogenetic characteristics of bat communities in human-modified landscapes.

BACKGROUND: Assembly of species into communities following human disturbance (e.g., deforestation, fragmentation) may be governed by spatial (e.g., dispersal) or environmental (e.g., niche partitioning) mechanisms. Variation partitioning has been used to broadly disentangle spatial and environmental mechanisms, and approaches utilizing functional and phylogenetic characteristics of communities have been implemented to determine the relative importance of particular environmental (or niche-based) mechanisms. Nonetheless, few studies have integrated these quantitative approaches to comprehensively assess the relative importance of particular structuring processes. METHODS: We employed a novel variation partitioning approach to evaluate the relative importance of particular spatial and environmental drivers of taxonomic, functional, and phylogenetic aspects of bat communities in a human-modified landscape in Costa Rica. Specifically, we estimated the amount of variation in species composition (taxonomic structure) and in two aspects of functional and phylogenetic structure (i.e., composition and dispersion) along a forest loss and fragmentation gradient that are uniquely explained by landscape characteristics (i.e., environment) or space to assess the importance of competing mechanisms. RESULTS: The unique effects of space on taxonomic, functional and phylogenetic structure were consistently small. In contrast, landscape characteristics (i.e., environment) played an appreciable role in structuring bat communities. Spatially-structured landscape characteristics explained 84% of the variation in functional or phylogenetic dispersion, and the unique effects of landscape characteristics significantly explained 14% of the variation in species composition. Furthermore, variation in bat community structure was primarily due to differences in dispersion of species within functional or phylogenetic space along the gradient, rather than due to differences in functional or phylogenetic composition. DISCUSSION: Variation among bat communities was related to environmental mechanisms, especially niche-based (i.e., environmental) processes, rather than spatial mechanisms. High variation in functional or phylogenetic dispersion, as opposed to functional or phylogenetic composition, suggests that loss or gain of niche space is driving the progressive loss or gain of species with particular traits from communities along the human-modified gradient. Thus, environmental characteristics associated with landscape structure influence functional or phylogenetic aspects of bat communities by effectively altering the ways in which species partition niche space.

Standardized Assessment of Biodiversity Trends in Tropical Forest Protected Areas: The End Is Not in Sight.

Extinction rates in the Anthropocene are three orders of magnitude higher than background and disproportionately occur in the tropics, home of half the world's species. Despite global efforts to combat tropical species extinctions, lack of high-quality, objective information on tropical biodiversity has hampered quantitative evaluation of conservation strategies. In particular, the scarcity of population-level monitoring in tropical forests has stymied assessment of biodiversity outcomes, such as the status and trends of animal populations in protected areas. Here, we evaluate occupancy trends for 511 populations of terrestrial mammals and birds, representing 244 species from 15 tropical forest protected areas on three continents. For the first time to our knowledge, we use annual surveys from tropical forests worldwide that employ a standardized camera trapping protocol, and we compute data analytics that correct for imperfect detection. We found that occupancy declined in 22%, increased in 17%, and exhibited no change in 22% of populations during the last 3-8 years, while 39% of populations were detected too infrequently to assess occupancy changes. Despite extensive variability in occupancy trends, these 15 tropical protected areas have not exhibited systematic declines in biodiversity (i.e., occupancy, richness, or evenness) at the community level. Our results differ from reports of widespread biodiversity declines based on aggregated secondary data and expert opinion and suggest less extreme deterioration in tropical forest protected areas. We simultaneously fill an important conservation data gap and demonstrate the value of large-scale monitoring infrastructure and powerful analytics, which can be scaled to incorporate additional sites, ecosystems, and monitoring methods. In an era of catastrophic biodiversity loss, robust indicators produced from standardized monitoring infrastructure are critical to accurately assess population outcomes and identify conservation strategies that can avert biodiversity collapse.

Bird biodiversity assessments in temperate forest: the value of point count versus acoustic monitoring protocols.

Effective monitoring programs for biodiversity are needed to assess trends in biodiversity and evaluate the consequences of management. This is particularly true for birds and faunas that occupy interior forest and other areas of low human population density, as these are frequently under-sampled compared to other habitats. For birds, Autonomous Recording Units (ARUs) have been proposed as a supplement or alternative to point counts made by human observers to enhance monitoring efforts. We employed two strategies (i.e., simultaneous-collection and same-season) to compare point count and ARU methods for quantifying species richness and composition of birds in temperate interior forests. The simultaneous-collection strategy compares surveys by ARUs and point counts, with methods matched in time, location, and survey duration such that the person and machine simultaneously collect data. The same-season strategy compares surveys from ARUs and point counts conducted at the same locations throughout the breeding season, but methods differ in the number, duration, and frequency of surveys. This second strategy more closely follows the ways in which monitoring programs are likely to be implemented. Site-specific estimates of richness (but not species composition) differed between methods; however, the nature of the relationship was dependent on the assessment strategy. Estimates of richness from point counts were greater than estimates from ARUs in the simultaneous-collection strategy. Woodpeckers in particular, were less frequently identified from ARUs than point counts with this strategy. Conversely, estimates of richness were lower from point counts than ARUs in the same-season strategy. Moreover, in the same-season strategy, ARUs detected the occurrence of passerines at a higher frequency than did point counts. Differences between ARU and point count methods were only detected in site-level comparisons. Importantly, both methods provide similar estimates of species richness and composition for the region. Consequently, if single visits to sites or short-term monitoring are the goal, point counts will likely perform better than ARUs, especially if species are rare or vocalize infrequently. However, if seasonal or annual monitoring of sites is the goal, ARUs offer a viable alternative to standard point-count methods, especially in the context of large-scale or long-term monitoring of temperate forest birds.

Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats.

Fragmentation per se due to human land conversion is a landscape-scale phenomenon. Accordingly, assessment of distributional patterns across a suite of potentially connected communities (i.e. metacommunity structure) is an appropriate approach for understanding the effects of landscape modification and complements the plethora of fragmentation studies that have focused on local community structure. To date, metacommunity structure within human-modified landscapes has been assessed with regard to nestedness along species richness gradients. This is problematic because there is little support that species richness gradients are associated with the factors moulding species distributions. More importantly, many alternative patterns are possible, and different patterns may manifest during different seasons and for different guilds because of variation in resource availability and resource requirements of taxa. We determined the best-fit metacommunity structure of a phyllostomid bat assemblage, frugivore ensemble, and gleaning animalivore ensemble within a human-modified landscape in the Caribbean lowlands of Costa Rica during the dry and wet seasons to elucidate important structuring mechanisms. Furthermore, we identified the landscape characteristics associated with the latent gradient underlying metacommunity structure. We discriminated among multiple metacommunity structures by assessing coherence, range turnover, and boundary clumping of an ordinated site-by-species matrix. We identified the landscape characteristics associated with the latent gradient underlying metacommunity structure via hierarchical partitioning. Metacommunity structure was never nested nor structured along a richness gradient. The phyllostomid assemblage and frugivore ensemble exhibited Gleasonian structure (range turnover along a common gradient) during the dry season and Clementsian structure (range turnover and shared boundaries along a common gradient) during the wet season. Distance between forest patches and forest edge density structured the phyllostomid metacommunity during the dry and wet seasons, respectively. Proportion of pasture and forest patch density structured the frugivore metacommunity during the dry season. Gleaning animalivores exhibited chequerboard structure (mutually exclusive species pairs) during the dry season and random structure during the wet season. Metacommunity structure was likely mediated by differential resource use or interspecific relationships. Furthermore, the interaction between landscape characteristics and seasonal variation in resources resulted in season-specific and guild-specific distributional patterns.

Evaluation of an integrated framework for biodiversity with a new metric for functional dispersion.

Growing interest in understanding ecological patterns from phylogenetic and functional perspectives has driven the development of metrics that capture variation in evolutionary histories or ecological functions of species. Recently, an integrated framework based on Hill numbers was developed that measures three dimensions of biodiversity based on abundance, phylogeny and function of species. This framework is highly flexible, allowing comparison of those diversity dimensions, including different aspects of a single dimension and their integration into a single measure. The behavior of those metrics with regard to variation in data structure has not been explored in detail, yet is critical for ensuring an appropriate match between the concept and its measurement. We evaluated how each metric responds to particular data structures and developed a new metric for functional biodiversity. The phylogenetic metric is sensitive to variation in the topology of phylogenetic trees, including variation in the relative lengths of basal, internal and terminal branches. In contrast, the functional metric exhibited multiple shortcomings: (1) species that are functionally redundant contribute nothing to functional diversity and (2) a single highly distinct species causes functional diversity to approach the minimum possible value. We introduced an alternative, improved metric based on functional dispersion that solves both of these problems. In addition, the new metric exhibited more desirable behavior when based on multiple traits.

Multiple dimensions of bat biodiversity along an extensive tropical elevational gradient.

Research concerning spatial dynamics of biodiversity generally has been limited to considerations of the taxonomic dimension, which is insensitive to interspecific variation in ecological or evolutionary characteristics that play important roles in species assembly and provide linkages to ecosystem services. Consequently, the assumption that the taxonomic dimension is a good surrogate for other dimensions remains unconfirmed. We assessed variation in taxonomic (species richness) as well as phylogenetic and functional (Rao's quadratic entropy, a measurement of dispersion) dimensions of bat biodiversity along an elevational gradient in the Manu Biosphere Reserve of Peru. Phylogenetic dispersion was based on relatedness of species derived from a mammalian supertree. Functional dispersion was estimated separately for each of six functional components that reflect particular niche axes (e.g. diet, foraging strategy, body size) and for all functional components combined. Species richness declined nonlinearly with elevation, whereas phylogenetic dispersion and functional dispersion based on all functional components were not significantly associated with elevation (orthogonal polynomial regression). Moreover, considerable heterogeneity in the form of elevational relationships existed among functional components. After accounting for variation in species richness, dispersion of phylogenetic, diet and foraging strategy attributes were significantly greater than expected at high elevations, whereas dispersion of body size was significantly less than expected at high elevations. Species richness was a poor surrogate for phylogenetic or functional dispersion. Functional dispersion based on multiple components obscured patterns detected by particular components and hindered identification of mechanistic explanations for elevational variation in biodiversity. Variation in phylogenetic dispersion effectively captured the composite variation represented by all functional components, suggesting a phylogenetic signal in functional attributes. Mechanisms that give rise to variation in richness do not fully account for variation in phylogenetic or functional characteristics of assemblages. Greater than expected phylogenetic, diet and foraging strategy dispersion at high elevations were associated with the loss of phylogenetically or functionally redundant species, suggesting that increasing interspecific competition with decreasing productivity resulted in competitive exclusion. In contrast, low dispersion of size attributes at high elevations suggests the importance of abiotic filtering that favours small-sized species that can more easily enter torpor.

Updating categorical soil maps using limited survey data by Bayesian Markov chain cosimulation.

Updating categorical soil maps is necessary for providing current, higher-quality soil data to agricultural and environmental management but may not require a costly thorough field survey because latest legacy maps may only need limited corrections. This study suggests a Markov chain random field (MCRF) sequential cosimulation (Co-MCSS) method for updating categorical soil maps using limited survey data provided that qualified legacy maps are available. A case study using synthetic data demonstrates that Co-MCSS can appreciably improve simulation accuracy of soil types with both contributions from a legacy map and limited sample data. The method indicates the following characteristics: (1) if a soil type indicates no change in an update survey or it has been reclassified into another type that similarly evinces no change, it will be simply reproduced in the updated map; (2) if a soil type has changes in some places, it will be simulated with uncertainty quantified by occurrence probability maps; (3) if a soil type has no change in an area but evinces changes in other distant areas, it still can be captured in the area with unobvious uncertainty. We concluded that Co-MCSS might be a practical method for updating categorical soil maps with limited survey data.