Standardized ethograms and a device for assessing amphibian thermal responses in a warming world

Most predictions of how populations and species of ectotherms will respond to global warming are based on estimates of the temperature at which organisms lose motor control (i.e., CT_max - the Critical Thermal Maximum). Here, we describe a non-lethal protocol and ethograms to estimate the relative tolerance of amphibians to increasing temperatures. These methods—suitable for field or laboratory conditions—are replicable, inexpensive and applicable to both post-metamorphic stages and organisms with direct development. We illustrate the use of this standardized protocol for four amphibians from a tropical cloud forest in Veracruz, Mexico with contrasting life histories: a lungless salamander (Aquiloeurycea cafetalera: Plethodontidae), a leaf-litter frog (Craugastor rhodopis: Craugastoridae), a semiaquatic frog (Lithobates berlandieri: Ranidae), and a tree frog (Rheohyla miotympanum: Hylidae). We identified four behavioral responses preceding CT_max for all amphibians included in this study: 1) Optimal Activity Range, 2) Supra-optimal Activity Range, 3) Heat Stress Range, and 4) Involuntary Movements Range. Additionally, we identified a fifth parameter associated with resilience to heat shock: 5) Recovery Stage after reaching CT_max. We conclude that the behavioral responses preceding the Critical Thermal Maximum are as informative as CT_max. Using behavioral responses to estimate thermal tolerance has the additional advantage of reducing the risk of injury or death of amphibians during physiological experiments.     

Effects of inbreeding on life history and thermal performance in the tropical butterfly Bicyclus anynana

Human-induced loss and fragmentation of natural habitats reduces population size and thereby presumably genetic diversity through inbreeding or genetic drift. Additionally, many species are confronted with increased temperature stress due to climate change, with reduced genetic diversity potentially interfering with a species’ ability to cope with such conditions. While in general the detrimental impact of inbreeding has often been documented, its consequences for the ability to cope with temperature stress are still poorly understood. Against this background we here investigate the effects of inbreeding on egg hatching success, development and temperature stress tolerance in the tropical butterfly Bicyclus anynana. Specifically we test for an increased sensitivity to environmental stress in inbred individuals. Our results revealed that even comparatively low levels of inbreeding yield negative consequences for reproduction and development under beneficial conditions. Inbreeding also reduced cold tolerance in adult butterflies, while heat tolerance remained unaffected. We therefore conclude that acute stress tolerance may not be generally impaired by inbreeding.     

Growth and physiological responses in largemouth bass populations to environmental warming: Effects of inhabiting chronically heated environments

Ectotherms are susceptible to increasing environmental temperatures associated with anthropogenic warming. Supra-optimum temperatures lead to declining aerobic capacity and can increase exposure to lethal temperatures, resulting in reduced performance. Although the capacity of phenotypic plasticity to minimize the effects of temperature on physiological processes is well studied, evidence of generational changes (e.g. transgenerational plasticity and rapid adaptation) in response to environmental warming is limited in natural populations. We investigated metabolism, growth, and thermal tolerance of largemouth bass (Micropterus salmoides) populations inhabiting thermally altered lakes (i.e. power plant cooling lakes) which have year-round elevated temperature regimes and exhibit supra-optimum temperatures on a yearly basis, and compared these traits with those in largemouth bass populations from ambient lakes. Largemouth bass from ambient and heated groups (n = 3 populations per group) were spawned in an ambient, common garden pond environment, then acclimated to either a normal summertime temperature (24 °C) or a supra-optimum temperature (30 °C). Fish from heated populations had significant reductions in the resting metabolic rate at both temperatures and markedly increased growth rates at 30 °C. By comparing pond-raised fish to fish removed directly from heated lakes, we showed that developmental plasticity played little role in establishing the metabolic rate. A lower resting metabolic rate contributed to an increase in the conversion efficiency of food to biomass of largemouth bass from heated lakes, regardless of temperature. Despite inhabiting heated lakes for many decades, neither critical thermal maximum nor minimum were altered in heated populations when raised in a common garden environment. These results suggest that largemouth bass can lessen sub-lethal effects of warming by altering physiological processes to reduce the impact of warming on aerobic scope and that these changes are generationally transient, but changes in maximum thermal tolerance in response to warming is limited to phenotypic plasticity.     

Too cold is better than too hot: Preferred temperatures and basking behaviour in a tropical freshwater turtle

Thermoregulation is critical to the survival of animals. Tropical environments can be particularly thermally challenging as they reach very high, even lethal, temperatures. The thermoregulatory responses of tropical freshwater turtles to these challenges are poorly known. One common thermoregulatory behaviour is diurnal basking, which, for many species, facilitates heat gain. Recently, however, a north-eastern Australian population of Krefft's river turtles (Emydura macquarii krefftii) has been observed basking nocturnally, possibly to allow cooling. To test this, we determined the thermal preference (central 50% of temperatures selected) of E. m. krefftii in an aquatic thermal gradient in the laboratory. We then conducted a manipulative experiment to test the effects of water temperatures, both lower and higher than preferred temperature, on diurnal and nocturnal basking. The preferred temperature range fell between 25.3°C (±SD: 1.5) and 27.6°C (±1.4) during the day, and 25.3°C (±2.4) and 26.8°C (±2.5) at night. Based on this, we exposed turtles to three 24 h water temperature treatments (‘cool’ [23°C], ‘preferred’ [26°C] and ‘warm’ [29°C]) while air temperature remained constant at 26°C. Turtles basked more frequently and for longer periods during both the day and night when water temperatures were above their preferred range (the ‘warm’ treatment). This population frequently encounters aquatic temperatures above the preferred thermal range, and our results support the hypothesis that nocturnal basking is a mechanism for escaping unfavourably warm water. Targeted field studies would be a valuable next step in understanding the seasonal scope of this behaviour in a natural environment.     

Insect responses to heat: physiological mechanisms,evolution and ecological implications in a warming world

Surviving changing climate conditions is particularly difficult for organisms such as insects that depend on environmental temperature to regulate their physiological functions. Insects are extremely threatened by global warming, since many do not have enough physiological tolerance even to survive continuous exposure to the current maximum temperatures experienced in their habitats. Here, we review literature on the physiological mechanisms that regulate responses to heat and provide heat tolerance in insects: (i) neuronal mechanisms to detect and respond to heat; (ii) metabolic responses to heat; (iii) thermoregulation; (iv) stress responses to tolerate heat; and (v) hormones that coordinate developmental and behavioural responses at warm temperatures. Our review shows that, apart from the stress response mediated by heat shock proteins, the physiological mechanisms of heat tolerance in insects remain poorly studied. Based on life‐history theory, we discuss the costs of heat tolerance and the potential evolutionary mechanisms driving insect adaptations to high temperatures. Some insects may deal with ongoing global warming by the joint action of phenotypic plasticity and genetic adaptation. Plastic responses are limited and may not be by themselves enough to withstand ongoing warming trends. Although the evidence is still scarce and deserves further research in different insect taxa, genetic adaptation to high temperatures may result from rapid evolution. Finally, we emphasize the importance of incorporating physiological information for modelling species distributions and ecological interactions under global warming scenarios. This review identifies several open questions to improve our understanding of how insects respond physiologically to heat and the evolutionary and ecological consequences of those responses. Further lines of research are suggested at the species, order and class levels, with experimental and analytical approaches such as artificial selection, quantitative genetics and comparative analyses.     

Differences in egg thermotolerance between tropical and temperate populations of the migratory locust Locusta migratoria (Orthoptera: Acridiidae)

The migratory locust Locusta migratoria L., which is widely distributed throughout the world, exhibits within- and between-population variation in cold tolerance. To understand physiological adaptation in populations, we studied the genetic basis of thermotolerance in Hainan (tropical) and Liaoning (temperate) populations and measured expression of Hsp70 and Hsp90 mRNA in both populations at low (0 degrees C) and high temperatures (40 degrees C). Phenotypic variation of thermotolerance is heritable. Heritable characteristics differed among different stages of locust egg development, as well as among different measures of thermotolerance. Nuclear genetic factors, rather than cytoplasmic factors, contribute to differences in cold tolerance between the tropical and temperate populations of the migratory locust; for heat tolerance, maternal effects were involved in three stages of egg development. Expression of Hsp90 mRNA was induced in temperate population after heat shock (40 degrees C x 12h), whereas expression of Hsp70 and 90 was induced in tropical population after cold shock (0 degrees C x 12h). We suggest that thermotolerance of locust eggs has a complex genetic basis and heat shock proteins may be involved in differences of thermotolerance between locust populations.     

Taxonomic challenges in freshwater fishes: a mismatch between morphology and DNA barcoding in fish of the north‐eastern part of the Congo basin

This study evaluates the utility of DNA barcoding to traditional morphology‐based species identifications for the fish fauna of the north‐eastern Congo basin. We compared DNA sequences (COI) of 821 samples from 206 morphologically identified species. Best match, best close match and all species barcoding analyses resulted in a rather low identification success of 87.5%, 84.5% and 64.1%, respectively. The ratio ‘nearest‐neighbour distance/maximum intraspecific divergence’ was lower than 1 for 26.1% of the samples, indicating possible taxonomic problems. In ten genera, belonging to six families, the number of species inferred from mtDNA data exceeded the number of species identified using morphological features; and in four cases indications of possible synonymy were detected. Finally, the DNA barcodes confirmed previously known identification problems within certain genera of the Clariidae, Cyprinidae and Mormyridae. Our results underscore the large number of taxonomic problems lingering in the taxonomy of the fish fauna of the Congo basin and illustrate why DNA barcodes will contribute to future efforts to compile a reliable taxonomic inventory of the Congo basin fish fauna. Therefore, the obtained barcodes were deposited in the reference barcode library of the Barcode of Life Initiative.     

The costs of keeping cool in a warming world: implications of high temperatures for foraging,thermoregulation and body condition of an arid‐zone bird

Recent mass mortalities of bats, birds and even humans highlight the substantial threats that rising global temperatures pose for endotherms. Although less dramatic, sublethal fitness costs of high temperatures may be considerable and result in changing population demographics. Endothermic animals exposed to high environmental temperatures can adjust their behaviour (e.g. reducing activity) or physiology (e.g. elevating rates of evaporative water loss) to maintain body temperatures within tolerable limits. The fitness consequences of these adjustments, in terms of the ability to balance water and energy budgets and therefore maintain body condition, are poorly known. We investigated the effects of daily maximum temperature on foraging and thermoregulatory behaviour as well as maintenance of body condition in a wild, habituated population of Southern Pied Babblers Turdoides bicolor. These birds inhabit a hot, arid area of southern Africa where they commonly experience environmental temperatures exceeding optimal body temperatures. Repeated measurements of individual behaviour and body mass were taken across days varying in maximum air temperature. Contrary to expectations, foraging effort was unaffected by daily maximum temperature. Foraging efficiency, however, was lower on hotter days and this was reflected in a drop in body mass on hotter days. When maximum air temperatures exceeded 35.5 °C, individuals no longer gained sufficient weight to counter typical overnight weight loss. This reduction in foraging efficiency is likely driven, in part, by a trade‐off with the need to engage in heat‐dissipation behaviours. When we controlled for temperature, individuals that actively dissipated heat while continuing to forage experienced a dramatic decrease in their foraging efficiency. This study demonstrates the value of investigations of temperature‐dependent behaviour in the context of impacts on body condition, and suggests that increasingly high temperatures will have negative implications for the fitness of these arid‐zone birds.     

Multiple host use by the egg parasitoid Trissolcus basalis (Wollaston) in a soybean agricultural system: biological control and environmental implications

1 Species of bugs (Hemiptera: Pentatomidae and other families) that are parasitized by the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in the soybean agricultural system on the Darling Downs in south-eastern Queensland, Australia, are reported. The degree to which eggs of each bug species are used by T. basalis is quantified, which allows assessment of the role of these alternative host species in the biological control of the green vegetable bug Nezara viridula (L.). 2 Egg masses of nine species of pentatomid bugs and one unidentified bug species were collected. Parasitism rates of egg masses of all species averaged 50–70% but were significantly lower for the more important pest species, including the green vegetable bug, than for some of the agriculturally less important species. 3 Trissolcus basalis emerged from nearly all species collected and was the major parasitoid to emerge from most species. A number of native species were parasitized heavily by T. basalis and parasitism of such species may enhance biological control of the green vegetable bug, but may also pose environmental concerns. Parasitism of predatory bugs by T. basalis may have a negative impact on the biological control of other pests, especially lepidopterous pests. 4 Although the impact of T. basalis on native and predatory host species was not directly quantified, these host species remain abundant and therefore do not appear to be affected adversely by such high rates of parasitism.     

Drought resistance in early and late secondary successional species from a tropical dry forest: the interplay between xylem resistance to embolism,sapwood water storage and leaf shedding

The mechanisms of drought resistance that allow plants to successfully establish at different stages of secondary succession in tropical dry forests are not well understood. We characterized mechanisms of drought resistance in early and late‐successional species and tested whether risk of drought differs across sites at different successional stages, and whether early and late‐successional species differ in resistance to experimentally imposed soil drought. The microenvironment in early successional sites was warmer and drier than in mature forest. Nevertheless, successional groups did not differ in resistance to soil drought. Late‐successional species resisted drought through two independent mechanisms: high resistance of xylem to embolism, or reliance on high stem water storage capacity. High sapwood water reserves delayed the effects of soil drying by transiently decoupling plant and soil water status. Resistance to soil drought resulted from the interplay between variations in xylem vulnerability to embolism, reliance on sapwood water reserves and leaf area reduction, leading to a tradeoff of avoidance against tolerance of soil drought, along which successional groups were not differentiated. Overall, our data suggest that ranking species' performance under soil drought based solely on xylem resistance to embolism may be misleading, especially for species with high sapwood water storage capacity.