Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Lucy Alford; Sacha  Roudine; Jean-Sébastien  Pierre; Françoise  Burel; Joan van Baaren

doi:10.1111/1744-7917.13044

Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Lucy Alford^*
, Sacha Roudine
, Jean-Sébastien Pierre
, Françoise Burel
, Joan van Baaren

^*Corresponding author for this work

School of Biological Sciences

Research output: Contribution to journal › Article (Academic Journal) › peer-review

3 Citations (Scopus)

26 Downloads (Pure)

Abstract

Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CTmin and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.

Original language	English
Pages (from-to)	251-263
Number of pages	13
Journal	Insect science
Volume	30
Issue number	1
Early online date	19 Apr 2022
DOIs	https://doi.org/10.1111/1744-7917.13044
Publication status	Published - 8 Feb 2023

Bibliographical note

Funding Information:
The authors gratefully acknowledge Mathilde Méheut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, Kévin Tougeron, Annabelle Androdias, Cécile Carré, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Valérie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Skłodowska‐Curie Actions Intra‐European Fellowship for the project “Climland” (FP7‐PEOPLE‐2012‐IEF‐326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020‐MSCA‐IF‐2018‐841952) awarded to L. Alford and J. van Baaren.

Funding Information:
The authors gratefully acknowledge Mathilde Méheut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, Kévin Tougeron, Annabelle Androdias, Cécile Carré, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Valérie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Skłodowska-Curie Actions Intra-European Fellowship for the project “Climland” (FP7-PEOPLE-2012-IEF-326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020-MSCA-IF-2018-841952) awarded to L. Alford and J. van Baaren.

Publisher Copyright:
© 2022 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

Keywords

agroecosystems
local adaptation
physiological thermal tolerance
plasticity
winter resistance

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title = "Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation",

abstract = "Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CTmin and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.",

keywords = "agroecosystems, local adaptation, physiological thermal tolerance, plasticity, winter resistance",

author = "Lucy Alford and Sacha Roudine and Jean-S{\'e}bastien Pierre and Fran{\c c}oise Burel and \{van Baaren\}, Joan",

note = "Funding Information: The authors gratefully acknowledge Mathilde M{\'e}heut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, K{\'e}vin Tougeron, Annabelle Androdias, C{\'e}cile Carr{\'e}, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Val{\'e}rie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Sk{\l}odowska‐Curie Actions Intra‐European Fellowship for the project “Climland” (FP7‐PEOPLE‐2012‐IEF‐326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020‐MSCA‐IF‐2018‐841952) awarded to L. Alford and J. van Baaren. Funding Information: The authors gratefully acknowledge Mathilde M{\'e}heut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, K{\'e}vin Tougeron, Annabelle Androdias, C{\'e}cile Carr{\'e}, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Val{\'e}rie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Sk{\l}odowska-Curie Actions Intra-European Fellowship for the project “Climland” (FP7-PEOPLE-2012-IEF-326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020-MSCA-IF-2018-841952) awarded to L. Alford and J. van Baaren. Publisher Copyright: {\textcopyright} 2022 The Authors. Insect Science published by John Wiley \& Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.",

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doi = "10.1111/1744-7917.13044",

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T1 - Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

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AU - Roudine, Sacha

AU - Pierre, Jean-Sébastien

AU - Burel, Françoise

AU - van Baaren, Joan

N1 - Funding Information: The authors gratefully acknowledge Mathilde Méheut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, Kévin Tougeron, Annabelle Androdias, Cécile Carré, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Valérie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Skłodowska‐Curie Actions Intra‐European Fellowship for the project “Climland” (FP7‐PEOPLE‐2012‐IEF‐326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020‐MSCA‐IF‐2018‐841952) awarded to L. Alford and J. van Baaren. Funding Information: The authors gratefully acknowledge Mathilde Méheut, Adrien Bonvin, Thomas Franco, Olivier Jambon, Romain Georges, Stephanie Llopis, Kévin Tougeron, Annabelle Androdias, Cécile Carré, Diab Al Hassan, and Charlotte Alford for assistance in the field. Thanks also to Stephanie Llopis for technical assistance, Valérie Briand for bibliographic assistance, and Sandra Rigaud for handling the administrative aspects of the grant. This study was funded by a Marie Skłodowska-Curie Actions Intra-European Fellowship for the project “Climland” (FP7-PEOPLE-2012-IEF-326943) awarded to L. Alford, F. Burel, and J. van Baaren and an Individual Fellowship for the project “FAB” (H2020-MSCA-IF-2018-841952) awarded to L. Alford and J. van Baaren. Publisher Copyright: © 2022 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

PY - 2023/2/8

Y1 - 2023/2/8

N2 - Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CTmin and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.

AB - Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CTmin and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.

KW - agroecosystems

KW - local adaptation

KW - physiological thermal tolerance

KW - plasticity

KW - winter resistance

U2 - 10.1111/1744-7917.13044

DO - 10.1111/1744-7917.13044

M3 - Article (Academic Journal)

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JO - Insect science

JF - Insect science

IS - 1

ER -

Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Abstract

Bibliographical note

Keywords

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