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Ecological implications of metabolic compensation at low temperatures in salamanders.

ABSTRACT: Global warming is influencing the biology of the world's biota. Temperature increases are occurring at a faster pace than that experienced by organisms in their evolutionary histories, limiting the organisms' response to new conditions. Mechanistic models that include physiological traits can help predict species' responses to warming. Changes in metabolism at high temperatures are often examined; yet many species are behaviorally shielded from high temperatures. Salamanders generally favor cold temperatures and are one of few groups of metazoans to be most species-rich in temperate regions. I examined variation in body temperature, behavioral activity, and temperature dependence of resting heart rate, used as a proxy for standard metabolic rate, in fire salamanders (Salamandra salamandra). Over 26 years, I found that salamanders are behaviorally active at temperatures as low as 1 °C, and aestivate at temperatures above 16 °C. Infrared thermography indicates limited thermoregulation opportunities for these nocturnal amphibians. Temperature affects resting heart rate, causing metabolic depression above 11 °C, and metabolic compensation below 8 °C: heart rate at 3 °C is 224% the expected heart rate. Thus, salamanders operating at low temperatures during periods of peak behavioral activity are able to maintain a higher metabolic rate than the rate expected in absence of compensation. This compensatory mechanism has important ecological implications, because it increases estimated seasonal heart rates. Increased heart rate, and thus metabolism, will require higher caloric intake for field-active salamanders. Thus, it is important to consider a species performance breadth over the entire temperature range, and particularly low temperatures that are ecologically relevant for cold tolerant species such as salamanders.

SUBMITTER: Catenazzi A

PROVIDER: S-EPMC4888306 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Ecological implications of metabolic compensation at low temperatures in salamanders.

Catenazzi Alessandro A

PeerJ 20160524

Global warming is influencing the biology of the world's biota. Temperature increases are occurring at a faster pace than that experienced by organisms in their evolutionary histories, limiting the organisms' response to new conditions. Mechanistic models that include physiological traits can help predict species' responses to warming. Changes in metabolism at high temperatures are often examined; yet many species are behaviorally shielded from high temperatures. Salamanders generally favor cold ...[more]

PMID: 27257549

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Project description:The analysis of transcriptomes is well-established and increasingly affordable in studies at the interface of ecology and evolution. Expression analysis of thousands of genes in parallel reveals functions and pathways involved in relevant phenotypic differentiation. The application of such methods typically involves the sacrifice of the analysed organisms, which is potentially subject to ethical and legal constraints. As an alternative to lethal sampling, transcriptome analyses can be performed using small biopsies of dispensable tissues. It has to be verified, however, to what extent such results are representative of the whole organism. Here, we use a custom microarray to compare transcriptomes of tail-clip samples with those of the remaining whole-body of fire salamander larvae (Salamandra salamandra). The microarray was calibrated using target RNA to validate the performance of each probe. We varied water temperature to test whether the thermal response in gene expression can be characterized in both types of sample. A large fraction (51 %) of the differentially expressed genes showed parallel changes for both tail clips and whole bodies in response to temperature. While sets of differentially expressed were not identical, they largely belonged to the same functional categories. The gene functions thus revealed a common thermal response of larvae irrespective of the sampled tissue. This included an overexpression of mitochondrial transcripts, an expected thermal acclimatization response of ectotherms. Hence, ecological transcriptomics based on small biopsies represent an alternative to the analysis of lethally sampled tissues in situations where the sacrifice of individuals is not an option. Larvae of European Fire salamander were exposed to two different temperatures (9°C & 17°C; n(cold) = 6, n(warm) = 6, n(total) = 12). The transcriptome response to temperature was assessed based on RNA extracted from tail tips, which can be sampled without sacrificing the individual, and based on RNA extracted from the remaining whole body. Results from the analysis of both tissues were compared.

Dataset Information

Ecological implications of metabolic compensation at low temperatures in salamanders.

Publications

Ecological implications of metabolic compensation at low temperatures in salamanders.

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