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.

Energy storage, body size and immune response of herbivore beetles at two different elevations in Costa Rica

The physiological condition and immune responses of organisms living at different elevations are expected to display local adaptations to the different climatic and biotic conditions. Small ectotherms with specialized diets are highly susceptible to environmental change, as their life cycle is largely affected by temperature and by the presence of specific resources. This study focuses on two species of rolled-leaf beetles (Chrysomelidae), both present at two different elevations in Costa Rica: Cephaloleia belti Baly, a diet-generalist, and Chelobasis bicolor Gray, a diet-specialist. Body size, energetic condition (lipid storage), muscle mass and immune condition (melanization response) were compared in beetle populations from a tropical rainforest (50 m elevation) and a tropical montane forest (2 000 m elevation). These measurements reflect current and past nutritional condition and hence are good estimators of individual fitness. We analyzed a total of 172 individuals from both species, sexes and elevations. We predicted that beetles at higher elevation would display larger body size, higher energetic condition and lower immune response associated with metabolic requirements and parasitic pressure in colder temperatures. In general, beetles at high altitude were larger, had more lipids and muscle and showed stronger melanization (i.e., immune response) than beetles at low altitudes. Such differences among populations at different elevations may reflect local adaptation to altitude or phenotypic plasticity. However, the effect of elevation was not equivalent amongst species or sex. Measuring physiological traits in organisms with broad elevational distributions could be useful in understanding possible species responses to climate change.

La condición fisiológica y la respuesta inmune de poblaciones que habitan a distintas altitudes pueden mostrar adaptación local a las condiciones abióticas y bióticas locales. Entre los organismos más susceptibles al cambio ambiental están los ectotermos pequeños con dietas especializadas, debido a que su ciclo de vida es, en gran medida, afectado tanto por la temperatura como por la presencia de recursos específicos. Este estudio se enfoca en dos especies de escarabajos (Chrysomelidae) presentes a lo largo de un gradiente altitudinal en Costa Rica: Cephaloleia belti Baly, una especie de dieta generalista, y Chelobasis bicolor Gray, de dieta especialista. Se comparó el tamaño corporal, la condición energética (almacenamiento de lípidos), la masa muscular y la condición inmunológica (respuesta de melanización) entre poblaciones de escarabajos de un bosque tropical (a 50 m de altitud) y un bosque tropical montano (a 2 000 m de altitud). Las variables seleccionadas reflejan las condiciones nutricionales actuales y pasadas y son buenos estimadores de la adecuación individual. Se analizaron un total de 172 escarabajos de ambas especies, sexos y elevaciones. Predecimos que los escarabajos a mayor elevación tendrán mayor tamaño corporal, mayor condición energética y menor respuesta inmune asociadas con los requerimientos metabólicos y la presión de los parásitos asociados con ambientes fríos. En general, los escarabajos a mayor altitud fueron más grandes, tuvieron más lípidos y masa muscular, y presentaron una mayor respuesta inmune de melanización que los escarabajos a menor altitud. Es posible que las diferencias entre las poblaciones a diferentes altitudes reflejen adaptaciones locales a las condiciones ambientales a distintas altitudes o plasticidad fenotípica. Sin embargo, el efecto de la altitud no fue de la misma magnitud entre las dos especies ni entre los dos sexos. La medición de caracteres fisiológicos en organismos ectotérmicos de amplia distribución altitudinal puede ser útil para entender las respuestas de ciertas especies al cambio climático.

Low quality diet and challenging temperatures affect vital rates, but not thermal tolerance in a tropical insect expanding its diet to an exotic plant.

Determining responses of organisms to changing temperatures is a research priority, as global warming threatens populations and ecosystems worldwide. Upper thermal limits are frequently measured as the critical thermal maximum (CTmax), a quick bioassay where organisms are exposed to increasing temperatures until individuals are not able to perform basic motor activities such as walking or flying. A more informative approach to understand organism responses to global warming is to evaluate how vital rates, such as growth or survival, change with temperatures. The main objectives of this study are: (1) to determine if factors affecting insect vital rates such as diet quality, developmental temperatures or acclimation also affect CTmax and (2) to determine if vital rates of different life stages (i.e., insect larvae or adults) display different responses to temperature changes. If different life stages have particular thermal requirements, this may indicate different susceptibility to global warming. This study focuses on Cephaloleia belti (Coleoptera: Chrysomelidae), a tropical insect currently expanding its diet to an exotic host plant. We determined how high and low-quality diets (i.e., native vs novel host), as well as exposure temperatures affect CTmax of adult beetles. We also estimated larval and adult survival when feeding on high and low quality host plants, when exposed to temperatures typical of the elevational distribution of this species, or when exposed to projected temperatures in 100 years. We did not detect an effect of diet quality or acclimation on CTmax. However, larvae and adults had different thermal requirements. CTmax is not affected by previous diet or acclimation as an adult. We propose that to understand processes involved in the adaptation and persistence of ectotherm populations in a warming world, studies must explore responses beyond CTmax, and focus on the response of vital rates to changing temperatures.

Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction.

The critical thermal maximum (CTmax), the temperature at which motor control is lost in animals, has the potential to determine if species will tolerate global warming. For insects, tolerance to high temperatures decreases with latitude, suggesting that similar patterns may exist along elevational gradients as well. This study explored how CTmax varies among species and populations of a group of diverse tropical insect herbivores, the rolled-leaf beetles, across both broad and narrow elevational gradients. Data from 6,948 field observations and 8,700 museum specimens were used to map the elevational distributions of rolled-leaf beetles on two mountains in Costa Rica. CTmax was determined for 1,252 individual beetles representing all populations across the gradients. Initial morphological identifications suggested a total of 26 species with populations at different elevations displaying contrasting upper thermal limits. However, compared with morphological identifications, DNA barcodes (cytochrome oxidase I) revealed significant cryptic species diversity. DNA barcodes identified 42 species and haplotypes across 11 species complexes. These 42 species displayed much narrower elevational distributions and values of CTmax than the 26 morphologically defined species. In general, species found at middle elevations and on mountaintops are less tolerant to high temperatures than species restricted to lowland habitats. Species with broad elevational distributions display high CTmax throughout their ranges. We found no significant phylogenetic signal in CTmax, geography, or elevational range. The narrow variance in CTmax values for most rolled-leaf beetles, especially high-elevation species, suggests that the risk of extinction of insects may be substantial under some projected rates of global warming.

Scatter hoarding of seeds confers survival advantages and disadvantages to large-seeded tropical plants at different life stages.

Scatter hoarding of seeds by animals contributes significantly to forest-level processes, including plant recruitment and forest community composition. However, the potential positive and negative effects of caching on seed survival, germination success, and seedling survival have rarely been assessed through experimental studies. Here, I tested the hypothesis that seed burial mimicking caches made by scatter hoarding Central American agoutis (Dasyprocta punctate) enhances seed survival, germination, and growth by protecting seeds from seed predators and providing favorable microhabitats for germination. In a series of experiments, I used simulated agouti seed caches to assess how hoarding affects seed predation by ground-dwelling invertebrates and vertebrates for four plant species. I tracked germination and seedling growth of intact and beetle-infested seeds and, using exclosures, monitored the effects of mammals on seedling survival through time. All experiments were conducted over three years in a lowland wet forest in Costa Rica. The majority of hoarded palm seeds escaped predation by both invertebrates and vertebrates while exposed seeds suffered high levels of infestation and removal. Hoarding had no effect on infestation rates of D. panamensis, but burial negatively affected germination success by preventing endocarp dehiscence. Non-infested palm seeds had higher germination success and produced larger seedlings than infested seeds. Seedlings of A. alatum and I. deltoidea suffered high mortality by seed-eating mammals. Hoarding protected most seeds from predators and enhanced germination success (except for D. panamensis) and seedling growth, although mammals killed many seedlings of two plant species; all seedling deaths were due to seed removal from the plant base. Using experimental caches, this study shows that scatter hoarding is beneficial to most seeds and may positively affect plant propagation in tropical forests, although tradeoffs in seed survival do exist.