Correction: Integrating tropical research into biology education is urgently needed.

[This corrects the article DOI: 10.1371/journal.pbio.3001674.].

Integrating tropical research into biology education is urgently needed.

Understanding tropical biology is important for solving complex problems such as climate change, biodiversity loss, and zoonotic pandemics, but biology curricula view research mostly via a temperate-zone lens. Integrating tropical research into biology education is urgently needed to tackle these issues.

A general pattern of trade-offs between ecosystem resistance and resilience to tropical cyclones.

Tropical cyclones drive coastal ecosystem dynamics, and their frequency, intensity, and spatial distribution are predicted to shift with climate change. Patterns of resistance and resilience were synthesized for 4138 ecosystem time series from n = 26 storms occurring between 1985 and 2018 in the Northern Hemisphere to predict how coastal ecosystems will respond to future disturbance regimes. Data were grouped by ecosystems (fresh water, salt water, terrestrial, and wetland) and response categories (biogeochemistry, hydrography, mobile biota, sedentary fauna, and vascular plants). We observed a repeated pattern of trade-offs between resistance and resilience across analyses. These patterns are likely the outcomes of evolutionary adaptation, they conform to disturbance theories, and they indicate that consistent rules may govern ecosystem susceptibility to tropical cyclones.

Haiti has more forest than previously reported: land change 2000-2015.

Estimates of forest cover have important political, conservation, and funding implications, but methods vary greatly. Haiti has often been cited as one of the most deforested countries in the world, yet estimates of forest cover range from <1% to 33%. Here, we analyze land change for seven land cover classes (forest, shrub land, agriculture/pasture, plantation, urban/infrastructure, barren land, and water) between 2000 and 2015 using Landsat imagery (30 m resolution) in the Google Earth Engine platform. Forest cover was estimated at 26% in 2000 and 21% in 2015. Although forest cover is declining in Haiti, our quantitative analysis resulted in considerably higher forest cover than what is usually reported by local and international institutions. Our results determined that areas of forest decline were mainly converted to shrubs and mixed agriculture/pasture. An important driver of forest loss and degradation could be the high demand for charcoal, which is the principal source of cooking fuel. Our results differ from other forest cover estimates and forest reports from national and international institutions, most likely due to differences in forest definition, data sources, spatial resolution, and methods. In the case of Haiti, this work demonstrates the need for clear and functional definitions and classification methods to accurately represent land use/cover change. Regardless of how forests are defined, forest cover in Haiti will continue to decline unless corrective actions are taken to protect remaining forest patches. This can serve as a warning of the destructive land use patterns and can help us target efforts for better planning, management, and conservation.

Biodiversity recovery of Neotropical secondary forests.

Old-growth tropical forests harbor an immense diversity of tree species but are rapidly being cleared, while secondary forests that regrow on abandoned agricultural lands increase in extent. We assess how tree species richness and composition recover during secondary succession across gradients in environmental conditions and anthropogenic disturbance in an unprecedented multisite analysis for the Neotropics. Secondary forests recover remarkably fast in species richness but slowly in species composition. Secondary forests take a median time of five decades to recover the species richness of old-growth forest (80% recovery after 20 years) based on rarefaction analysis. Full recovery of species composition takes centuries (only 34% recovery after 20 years). A dual strategy that maintains both old-growth forests and species-rich secondary forests is therefore crucial for biodiversity conservation in human-modified tropical landscapes.

Woody vegetation dynamics in the tropical and subtropical Andes from 2001 to 2014: Satellite image interpretation and expert validation.

The interactions between climate and land-use change are dictating the distribution of flora and fauna and reshuffling biotic community composition around the world. Tropical mountains are particularly sensitive because they often have a high human population density, a long history of agriculture, range-restricted species, and high-beta diversity due to a steep elevation gradient. Here we evaluated the change in distribution of woody vegetation in the tropical Andes of South America for the period 2001-2014. For the analyses we created annual land-cover/land-use maps using MODIS satellite data at 250 m pixel resolution, calculated the cover of woody vegetation (trees and shrubs) in 9,274 hexagons of 115.47 km2 , and then determined if there was a statistically significant (p < 0.05) 14 year linear trend (positive-forest gain, negative-forest loss) within each hexagon. Of the 1,308 hexagons with significant trends, 36.6% (n = 479) lost forests and 63.4% (n = 829) gained forests. We estimated an overall net gain of ~500,000 ha in woody vegetation. Forest loss dominated the 1,000-1,499 m elevation zone and forest gain dominated above 1,500 m. The most important transitions were forest loss at lower elevations for pastures and croplands, forest gain in abandoned pastures and cropland in mid-elevation areas, and shrub encroachment into highland grasslands. Expert validation confirmed the observed trends, but some areas of apparent forest gain were associated with new shade coffee, pine, or eucalypt plantations. In addition, after controlling for elevation and country, forest gain was associated with a decline in the rural population. Although we document an overall gain in forest cover, the recent reversal of forest gains in Colombia demonstrates that these coupled natural-human systems are highly dynamic and there is an urgent need of a regional real-time land-use, biodiversity, and ecosystem services monitoring network.

Legume abundance along successional and rainfall gradients in Neotropical forests.

The nutrient demands of regrowing tropical forests are partly satisfied by nitrogen-fixing legume trees, but our understanding of the abundance of those species is biased towards wet tropical regions. Here we show how the abundance of Leguminosae is affected by both recovery from disturbance and large-scale rainfall gradients through a synthesis of forest inventory plots from a network of 42 Neotropical forest chronosequences. During the first three decades of natural forest regeneration, legume basal area is twice as high in dry compared with wet secondary forests. The tremendous ecological success of legumes in recently disturbed, water-limited forests is likely to be related to both their reduced leaflet size and ability to fix N2, which together enhance legume drought tolerance and water-use efficiency. Earth system models should incorporate these large-scale successional and climatic patterns of legume dominance to provide more accurate estimates of the maximum potential for natural nitrogen fixation across tropical forests.

Have bird distributions shifted along an elevational gradient on a tropical mountain?

An upward shift in elevation is one of the most conspicuous species responses to climate change. Nevertheless, downward shifts and, apparently, the absences of response have also been recently reported. Given the growing evidence of multiple responses of species distributions due to climate change and the paucity of studies in the tropics, we evaluated the response of a montane bird community to climate change, without the confounding effects of land-use change. To test for elevational shifts, we compared the distribution of 21 avian species in 1998 and 2015 using occupancy models. The historical data set was based on point counts, whereas the contemporary data set was based on acoustic monitoring. We detected a similar number of species in historical (36) and contemporary data sets (33). We show an overall pattern of no significant change in range limits for most species, although there was a significant shift in the range limit of eight species (38%). Elevation limits shifted mostly upward, and this pattern was more common for upper than lower limits. Our results highlight the variability of species responses to climate change and illustrate how acoustic monitoring provides an easy and powerful way to monitor animal populations along elevational gradients.

Lowland extirpation of anuran populations on a tropical mountain.

BACKGROUND: Climate change and infectious diseases threaten animal and plant species, even in natural and protected areas. To cope with these changes, species may acclimate, adapt, move or decline. Here, we test for shifts in anuran distributions in the Luquillo Mountains (LM), a tropical montane forest in Puerto Rico by comparing species distributions from historical (1931-1989)and current data (2015/2016). METHODS: Historical data, which included different methodologies, were gathered through the Global Biodiversity Information Facility (GBIF) and published literature, and the current data were collected using acoustic recorders along three elevational transects. RESULTS: In the recordings, we detected the 12 native frog species known to occur in LM. Over a span of ∼25 years, two species have become extinct and four species suffered extirpation in lowland areas. As a consequence, low elevation areas in the LM (<300 m) have lost at least six anuran species. DISCUSSION: We hypothesize that these extirpations are due to the effects of climate change and infectious diseases, which are restricting many species to higher elevations and a much smaller area. Land use change is not responsible for these changes because LM has been a protected reserve for the past 80 years. However, previous studies indicate that (1) climate change has increased temperatures in Puerto Rico, and (2) Batrachochytrium dendrobatidis (Bd) was found in 10 native species and early detection of Bd coincides with anurans declines in the LM. Our study confirms the general impressions of amphibian population extirpations at low elevations, and corroborates the levels of threat assigned by IUCN.

A biodiversity hotspot losing its top predator: The challenge of jaguar conservation in the Atlantic Forest of South America.

The jaguar is the top predator of the Atlantic Forest (AF), which is a highly threatened biodiversity hotspot that occurs in Brazil, Paraguay and Argentina. By combining data sets from 14 research groups across the region, we determine the population status of the jaguar and propose a spatial prioritization for conservation actions. About 85% of the jaguar's habitat in the AF has been lost and only 7% remains in good condition. Jaguars persist in around 2.8% of the region, and live in very low densities in most of the areas. The population of jaguars in the AF is probably lower than 300 individuals scattered in small sub-populations. We identified seven Jaguar Conservation Units (JCUs) and seven potential JCUs, and only three of these areas may have ≥50 individuals. A connectivity analysis shows that most of the JCUs are isolated. Habitat loss and fragmentation were the major causes for jaguar decline, but human induced mortality is the main threat for the remaining population. We classified areas according to their contribution to jaguar conservation and we recommend management actions for each of them. The methodology in this study could be used for conservation planning of other carnivore species.

Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics.

Regrowth of tropical secondary forests following complete or nearly complete removal of forest vegetation actively stores carbon in aboveground biomass, partially counterbalancing carbon emissions from deforestation, forest degradation, burning of fossil fuels, and other anthropogenic sources. We estimate the age and spatial extent of lowland second-growth forests in the Latin American tropics and model their potential aboveground carbon accumulation over four decades. Our model shows that, in 2008, second-growth forests (1 to 60 years old) covered 2.4 million km(2) of land (28.1% of the total study area). Over 40 years, these lands can potentially accumulate a total aboveground carbon stock of 8.48 Pg C (petagrams of carbon) in aboveground biomass via low-cost natural regeneration or assisted regeneration, corresponding to a total CO2 sequestration of 31.09 Pg CO2. This total is equivalent to carbon emissions from fossil fuel use and industrial processes in all of Latin America and the Caribbean from 1993 to 2014. Ten countries account for 95% of this carbon storage potential, led by Brazil, Colombia, Mexico, and Venezuela. We model future land-use scenarios to guide national carbon mitigation policies. Permitting natural regeneration on 40% of lowland pastures potentially stores an additional 2.0 Pg C over 40 years. Our study provides information and maps to guide national-level forest-based carbon mitigation plans on the basis of estimated rates of natural regeneration and pasture abandonment. Coupled with avoided deforestation and sustainable forest management, natural regeneration of second-growth forests provides a low-cost mechanism that yields a high carbon sequestration potential with multiple benefits for biodiversity and ecosystem services.

Biomass resilience of Neotropical secondary forests.

Land-use change occurs nowhere more rapidly than in the tropics, where the imbalance between deforestation and forest regrowth has large consequences for the global carbon cycle. However, considerable uncertainty remains about the rate of biomass recovery in secondary forests, and how these rates are influenced by climate, landscape, and prior land use. Here we analyse aboveground biomass recovery during secondary succession in 45 forest sites and about 1,500 forest plots covering the major environmental gradients in the Neotropics. The studied secondary forests are highly productive and resilient. Aboveground biomass recovery after 20 years was on average 122 megagrams per hectare (Mg ha(-1)), corresponding to a net carbon uptake of 3.05 Mg C ha(-1) yr(-1), 11 times the uptake rate of old-growth forests. Aboveground biomass stocks took a median time of 66 years to recover to 90% of old-growth values. Aboveground biomass recovery after 20 years varied 11.3-fold (from 20 to 225 Mg ha(-1)) across sites, and this recovery increased with water availability (higher local rainfall and lower climatic water deficit). We present a biomass recovery map of Latin America, which illustrates geographical and climatic variation in carbon sequestration potential during forest regrowth. The map will support policies to minimize forest loss in areas where biomass resilience is naturally low (such as seasonally dry forest regions) and promote forest regeneration and restoration in humid tropical lowland areas with high biomass resilience.

Toward an integrated monitoring framework to assess the effects of tropical forest degradation and recovery on carbon stocks and biodiversity.

Tropical forests harbor a significant portion of global biodiversity and are a critical component of the climate system. Reducing deforestation and forest degradation contributes to global climate-change mitigation efforts, yet emissions and removals from forest dynamics are still poorly quantified. We reviewed the main challenges to estimate changes in carbon stocks and biodiversity due to degradation and recovery of tropical forests, focusing on three main areas: (1) the combination of field surveys and remote sensing; (2) evaluation of biodiversity and carbon values under a unified strategy; and (3) research efforts needed to understand and quantify forest degradation and recovery. The improvement of models and estimates of changes of forest carbon can foster process-oriented monitoring of forest dynamics, including different variables and using spatially explicit algorithms that account for regional and local differences, such as variation in climate, soil, nutrient content, topography, biodiversity, disturbance history, recovery pathways, and socioeconomic factors. Generating the data for these models requires affordable large-scale remote-sensing tools associated with a robust network of field plots that can generate spatially explicit information on a range of variables through time. By combining ecosystem models, multiscale remote sensing, and networks of field plots, we will be able to evaluate forest degradation and recovery and their interactions with biodiversity and carbon cycling. Improving monitoring strategies will allow a better understanding of the role of forest dynamics in climate-change mitigation, adaptation, and carbon cycle feedbacks, thereby reducing uncertainties in models of the key processes in the carbon cycle, including their impacts on biodiversity, which are fundamental to support forest governance policies, such as Reducing Emissions from Deforestation and Forest Degradation.

Real-time bioacoustics monitoring and automated species identification.

Traditionally, animal species diversity and abundance is assessed using a variety of methods that are generally costly, limited in space and time, and most importantly, they rarely include a permanent record. Given the urgency of climate change and the loss of habitat, it is vital that we use new technologies to improve and expand global biodiversity monitoring to thousands of sites around the world. In this article, we describe the acoustical component of the Automated Remote Biodiversity Monitoring Network (ARBIMON), a novel combination of hardware and software for automating data acquisition, data management, and species identification based on audio recordings. The major components of the cyberinfrastructure include: a solar powered remote monitoring station that sends 1-min recordings every 10 min to a base station, which relays the recordings in real-time to the project server, where the recordings are processed and uploaded to the project website (arbimon.net). Along with a module for viewing, listening, and annotating recordings, the website includes a species identification interface to help users create machine learning algorithms to automate species identification. To demonstrate the system we present data on the vocal activity patterns of birds, frogs, insects, and mammals from Puerto Rico and Costa Rica.

Contrasting patterns of urban expansion in Colombia, Ecuador, Peru, and Bolivia between 1992 and 2009.

The global urban population is increasing rapidly, but patterns of urban expansion differ greatly among countries. Urban transition theory predicts that the shift from low to high urbanization depends on a country's history and level of economic development. This study describes urban expansion in Colombia, Ecuador, Peru, and Bolivia between 1992 and 2009. Urban dynamics were analyzed by combining nighttime lights and census data from 4032 municipalities. High-lit areas (>52-63 pixel values) were correlated with urban populations across municipalities and years (R (2) > 0.90). Analyses showed that between 1992 and 2009 Bolivia and Ecuador had rapid population growth and rapidly increasing high-lit areas, while Peru and Colombia had lower rates of population growth and urbanization (i.e., expansion of high-lit areas). We demonstrate how nighttime lights can be a useful tool, providing a homogeneous platform for multi-scale analyses of urban growth.

Land cover change in Colombia: surprising forest recovery trends between 2001 and 2010.

BACKGROUND: Monitoring land change at multiple spatial scales is essential for identifying hotspots of change, and for developing and implementing policies for conserving biodiversity and habitats. In the high diversity country of Colombia, these types of analyses are difficult because there is no consistent wall-to-wall, multi-temporal dataset for land-use and land-cover change. METHODOLOGY/PRINCIPAL FINDINGS: To address this problem, we mapped annual land-use and land-cover from 2001 to 2010 in Colombia using MODIS (250 m) products coupled with reference data from high spatial resolution imagery (QuickBird) in Google Earth. We used QuickBird imagery to visually interpret percent cover of eight land cover classes used for classifier training and accuracy assessment. Based on these maps we evaluated land cover change at four spatial scales country, biome, ecoregion, and municipality. Of the 1,117 municipalities, 820 had a net gain in woody vegetation (28,092 km(2)) while 264 had a net loss (11,129 km(2)), which resulted in a net gain of 16,963 km(2) in woody vegetation at the national scale. Woody regrowth mainly occurred in areas previously classified as mixed woody/plantation rather than agriculture/herbaceous. The majority of this gain occurred in the Moist Forest biome, within the montane forest ecoregions, while the greatest loss of woody vegetation occurred in the Llanos and Apure-Villavicencio ecoregions. CONCLUSIONS: The unexpected forest recovery trend, particularly in the Andes, provides an opportunity to expand current protected areas and to promote habitat connectivity. Furthermore, ecoregions with intense land conversion (e.g. Northern Andean Páramo) and ecoregions under-represented in the protected area network (e.g. Llanos, Apure-Villavicencio Dry forest, and Magdalena-Urabá Moist forest ecoregions) should be considered for new protected areas.

Asymmetric forest transition driven by the interaction of socioeconomic development and environmental heterogeneity in Central America.

Forest transitions (FT) have been observed in many developed countries and more recently in the developing world. However, our knowledge of FT from tropical regions is mostly derived from case studies from within a particular country, making it difficult to generalize findings across larger regions. Here we overcome these difficulties by conducting a recent (2001-2010) satellite-based analysis of trends in forest cover across Central America, stratified by biomes, which we related to socioeconomic variables associated with human development. Results show a net decrease of woody vegetation resulting from 12,201 km(2) of deforestation of moist forests and 6,825 km(2) of regrowth of conifer and dry forests. The Human Development Index was the socioeconomic variable best associated with forest cover change. The least-developed countries, Nicaragua and Guatemala, experienced both rapid deforestation of moist forests and significant recovery of conifer and dry forests. In contrast, the most developed countries, Panama and Costa Rica, had net woody vegetation gain and a more stable forest cover configuration. These results imply a good agreement with FT predictions of forest change in relation to socioeconomic development, but strong asymmetry in rates and directions of change largely dependent upon the biome where change is occurring. The FT model should be refined by incorporating ecological and socioeconomic heterogeneity, particularly in multicountry and regional studies. These asymmetric patterns of forest change should be evaluated when developing strategies for conserving biodiversity and environmental services.

Implications of rural-urban migration for conservation of the Atlantic Forest and urban growth in Misiones, Argentina (1970-2030).

Global trends of increasing rural-urban migration and population urbanization could provide opportunities for nature conservation, particularly in regions where deforestation is driven by subsistence agriculture. We analyzed the role of rural population as a driver of deforestation and its contribution to urban population growth from 1970 to the present in the Atlantic Forest of Argentina, a global conservation priority. We created future land-use-cover scenarios based on human demographic parameters and the relationship between rural population and land-cover change between 1970 and 2006. In 2006, native forest covered 50% of the province, but by 2030 all scenarios predicted a decrease that ranged from 18 to 39% forest cover. Between 1970 and 2001, rural migrants represented 20% of urban population growth and are expected to represent less than 10% by 2030. This modeling approach shows how rural-urban migration and land-use planning can favor nature conservation with little impact on urban areas.

A contemporary assessment of change in humid tropical forests.

In recent decades the rate and geographic extent of land-use and land-cover change has increased throughout the world's humid tropical forests. The pan-tropical geography of forest change is a challenge to assess, and improved estimates of the human footprint in the tropics are critical to understanding potential changes in biodiversity. We combined recently published and new satellite observations, along with images from Google Earth and a literature review, to estimate the contemporary global extent of deforestation, selective logging, and secondary regrowth in humid tropical forests. Roughly 1.4% of the biome was deforested between 2000 and 2005. As of 2005, about half of the humid tropical forest biome contained 50% or less tree cover. Although not directly comparable to deforestation, geographic estimates of selective logging indicate that at least 20% of the humid tropical forest biome was undergoing some level of timber harvesting between 2000 and 2005. Forest recovery estimates are even less certain, but a compilation of available reports suggests that at least 1.2% of the humid tropical forest biome was in some stage of long-term secondary regrowth in 2000. Nearly 70% of the regrowth reports indicate forest regeneration in hilly, upland, and mountainous environments considered marginal for large-scale agriculture and ranching. Our estimates of the human footprint are conservative because they do not resolve very small-scale deforestation, low-intensity logging, and unreported secondary regrowth, nor do they incorporate other impacts on tropical forest ecosystems, such as fire and hunting. Our results highlight the enormous geographic extent of forest change throughout the humid tropics and the considerable limitations of the science and technology available for such a synthesis.