Effects of agriculture and nature reserves on avian behavior in northwestern Costa Rica.

Behavioral changes are often animals' first responses to environmental change and may act as a bellwether for population viability. Nonetheless, most studies of habitat conversion focus on changes in species occurrences or abundances. We analyzed >14,000 behavioral observations across 55 bird species in communities in northwestern Costa Rica to determine how land use affects reproductive, foraging, and other passive kinds of behaviors not associated with either foraging or reproduction. Specifically, we quantified differences in behaviors between farms, privately owned forests, and protected areas and implemented a novel modeling framework to account for variation in detection among behaviors. This framework entailed estimating abundances of birds performing different behaviors while allowing detection probabilities of individuals to vary by behavior. Birds were 1.2 times more likely to exhibit reproductive behaviors in forest than in agriculture and 1.5 times more likely to exhibit reproductive behaviors in protected areas than in private forests. Species were not always most abundant in the habitats where they were most likely to exhibit foraging or reproductive behaviors. Finally, species of higher conservation concern were less abundant in agriculture than in forest. Together, our results highlight the importance of behavioral analyses for elucidating the conservation value of different land uses.

Efectos de la agricultura y las reservas naturales sobre el comportamiento de las aves en el noroeste de Costa Rica Resumen Los cambios conductuales suelen ser la primera respuesta de los animales ante el cambio ambiental y pueden funcionar como un barómetro para la viabilidad poblacional. Sin embargo, la mayoría de los estudios sobre la conversión del hábitat se enfocan en cambios en la presencia o abundancia de las especies. Analizamos más de 14,000 observaciones conductuales en las comunidades de 55 especies de aves del noroeste de Costa Rica para determinar cómo el uso de suelo afectó el comportamiento reproductivo, de forrajeo y otras formas pasivas no asociadas con las dos anteriores. En específico, cuantificamos las diferencias en el comportamiento entre granjas, bosques de propiedad privada y áreas protegidas e implementamos un marco novedoso de modelado para justificar la variación en la detección entre los comportamientos. Este marco implicó estimar la abundancia de aves que realizaban diferentes comportamientos mientras permitía que variaran las probabilidades de detección de individuos según el comportamiento. Fue 1.2 veces más probable que las aves exhibieran comportamiento reproductivo en el bosque que en las zonas agrícolas y 1.5 veces más probable que exhibieran estos comportamientos en las áreas protegidas que en los bosques privados. Las especies no siempre fueron las más abundantes en los hábitats en donde era más probable que exhibieran comportamientos reproductivos o de forrajeo. Por último, las especies de mayor preocupación para la conservación fueron menos abundantes en las zonas agrícolas que en los bosques. En conjunto, nuestros resultados resaltan la importancia del análisis conductual para ilustrar el valor de conservación de los diferentes usos de suelo.

Publisher Correction: Intensive farming drives long-term shifts in avian community composition.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Intensive farming drives long-term shifts in avian community composition.

Agricultural practices constitute both the greatest cause of biodiversity loss and the greatest opportunity for conservation1,2, given the shrinking scope of protected areas in many regions. Recent studies have documented the high levels of biodiversity-across many taxa and biomes-that agricultural landscapes can support over the short term1,3,4. However, little is known about the long-term effects of alternative agricultural practices on ecological communities4,5 Here we document changes in bird communities in intensive-agriculture, diversified-agriculture and natural-forest habitats in 4 regions of Costa Rica over a period of 18 years. Long-term directional shifts in bird communities were evident in intensive- and diversified-agricultural habitats, but were strongest in intensive-agricultural habitats, where the number of endemic and International Union for Conservation of Nature (IUCN) Red List species fell over time. All major guilds, including those involved in pest control, pollination and seed dispersal, were affected. Bird communities in intensive-agricultural habitats proved more susceptible to changes in climate, with hotter and drier periods associated with greater changes in community composition in these settings. These findings demonstrate that diversified agriculture can help to alleviate the long-term loss of biodiversity outside natural protected areas1.

Agriculture erases climate-driven ß-diversity in Neotropical bird communities.

Earth is experiencing multiple global changes that will, together, determine the fate of many species. Yet, how biological communities respond to concurrent stressors at local-to-regional scales remains largely unknown. In particular, understanding how local habitat conversion interacts with regional climate change to shape patterns in ß-diversity-differences among sites in their species compositions-is critical to forecast communities in the Anthropocene. Here, we study patterns in bird ß-diversity across land-use and precipitation gradients in Costa Rica. We mapped forest cover, modeled regional precipitation, and collected data on bird community composition, vegetation structure, and tree diversity across 120 sites on 20 farms to answer three questions. First, do bird communities respond more strongly to changes in land use or climate in northwest Costa Rica? Second, does habitat conversion eliminate ß-diversity across climate gradients? Third, does regional climate control how communities respond to habitat conversion and, if so, how? After correcting for imperfect detection, we found that local land-use determined community shifts along the climate gradient. In forests, bird communities were distinct between sites that differed in vegetation structure or precipitation. In agriculture, however, vegetation structure was more uniform, contributing to 7%-11% less bird turnover than in forests. In addition, bird responses to agriculture and climate were linked: agricultural communities across the precipitation gradient shared more species with dry than wet forest communities. These findings suggest that habitat conversion and anticipated climate drying will act together to exacerbate biotic homogenization.

Climate change and habitat conversion favour the same species.

Land-use change and climate change are driving a global biodiversity crisis. Yet, how species' responses to climate change are correlated with their responses to land-use change is poorly understood. Here, we assess the linkages between climate and land-use change on birds in Neotropical forest and agriculture. Across > 300 species, we show that affiliation with drier climates is associated with an ability to persist in and colonise agriculture. Further, species shift their habitat use along a precipitation gradient: species prefer forest in drier regions, but use agriculture more in wetter zones. Finally, forest-dependent species that avoid agriculture are most likely to experience decreases in habitable range size if current drying trends in the Neotropics continue as predicted. This linkage suggests a synergy between the primary drivers of biodiversity loss. Because they favour the same species, climate and land-use change will likely homogenise biodiversity more severely than otherwise anticipated.

Loss of avian phylogenetic diversity in neotropical agricultural systems.

Habitat conversion is the primary driver of biodiversity loss, yet little is known about how it is restructuring the tree of life by favoring some lineages over others. We combined a complete avian phylogeny with 12 years of Costa Rican bird surveys (118,127 detections across 487 species) sampled in three land uses: forest reserves, diversified agricultural systems, and intensive monocultures. Diversified agricultural systems supported 600 million more years of evolutionary history than intensive monocultures but 300 million fewer years than forests. Compared with species with many extant relatives, evolutionarily distinct species were extirpated at higher rates in both diversified and intensive agricultural systems. Forests are therefore essential for maintaining diversity across the tree of life, but diversified agricultural systems may help buffer against extreme loss of phylogenetic diversity.

Intensive agriculture erodes ß-diversity at large scales.

Biodiversity is declining from unprecedented land conversions that replace diverse, low-intensity agriculture with vast expanses under homogeneous, intensive production. Despite documented losses of species richness, consequences for ß-diversity, changes in community composition between sites, are largely unknown, especially in the tropics. Using a 10-year data set on Costa Rican birds, we find that low-intensity agriculture sustained ß-diversity across large scales on a par with forest. In high-intensity agriculture, low local (α) diversity inflated ß-diversity as a statistical artefact. Therefore, at small spatial scales, intensive agriculture appeared to retain ß-diversity. Unlike in forest or low-intensity systems, however, high-intensity agriculture also homogenised vegetation structure over large distances, thereby decoupling the fundamental ecological pattern of bird communities changing with geographical distance. This ~40% decline in species turnover indicates a significant decline in ß-diversity at large spatial scales. These findings point the way towards multi-functional agricultural systems that maintain agricultural productivity while simultaneously conserving biodiversity.

Resilience and stability in bird guilds across tropical countryside.

The consequences of biodiversity decline in intensified agricultural landscapes hinge on surviving biotic assemblages. Maintaining crucial ecosystem processes and services requires resilience to natural and anthropogenic disturbances. However, the resilience and stability of surviving biological communities remain poorly quantified. From a 10-y dataset comprising 2,880 bird censuses across a land-use gradient, we present three key findings concerning the resilience and stability of Costa Rican bird communities. First, seed dispersing, insect eating, and pollinating guilds were more resilient to low-intensity land use than high-intensity land use. Compared with forest assemblages, bird abundance, species richness, and diversity were all ~15% lower in low-intensity land use and ~50% lower in high-intensity land use. Second, patterns in species richness generally correlated with patterns in stability: guilds exhibited less variation in abundance in low-intensity land use than in high-intensity land use. Finally, interspecific differences in reaction to environmental change (response diversity) and possibly the portfolio effect, but not negative covariance of species abundances, conferred resilience and stability. These findings point to the changes needed in agricultural production practices in the tropics to better sustain bird communities and, possibly, the functional and service roles that they play.