Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods

Summary 1. Ectotherms rely heavily on the spatial variance of environmental conditions to thermoregulate. Theoretically, their fitness is maximized when they can find suitable microhabitats by moving over short distances – this condition is met when spatial variance is high at fine spatial scales. Strikingly, despite the diversity of organisms living in leaf microhabitats, little is known about the impact of warming on the spatial variance of climatic conditions at the scale of individual leaf surfaces. 2. Here, we used experimental manipulation of ambient conditions to quantify the effects of environmental change on the thermal heterogeneity within individual leaf surfaces. We also explored the implications for behavioural thermoregulation by arthropods at a single leaf surface. 3. Using thermography, we characterized the apple leaf microclimate in terms of span and spatial aggregation of surface temperatures across a range of air temperatures and relative humidities. Then, we assessed how thermal heterogeneity within individual leaves affected behavioural thermoregulation by the two-spotted spider mite (Tetranychus urticae Koch) under both nearoptimal and sublethal conditions in this microhabitat. We measured the upper lethal temperature threshold of the mite to define sublethal exposure. 4. Thermal heterogeneity of individual leaves was driven mainly by ambient air temperature. Higher air temperatures gave both smaller ranges and higher spatial aggregation of temperatures at the leaf surface, such that the leaf microclimate was homogenized. 5. Tetranychus urticae used behavioural thermoregulation at moderate air temperature, when thermal heterogeneity was high at the leaf surface. At higher air temperature, however, heterogeneity declined and spider mites did not perform behavioural thermoregulation. 6. Warming decreases thermal heterogeneity of leaf surfaces with critical implications for arthropods – behavioural thermoregulation alone is not sufficient to escape the heat in the leaf microhabitat. Information on spatial variance of microclimatic conditions is critical for estimating how readily organisms can buffer global warming by moving.

[1]  Brett R. Scheffers,et al.  Microhabitats reduce animal's exposure to climate extremes , 2014, Global change biology.

[2]  M. Kearney,et al.  Activity restriction and the mechanistic basis for extinctions under climate warming. , 2013, Ecology letters.

[3]  H. Jones Plants and Microclimate: Other environmental factors: wind, altitude, climate change and atmospheric pollutants , 2013 .

[4]  H. Woods,et al.  Ontogenetic changes in the body temperature of an insect herbivore , 2013 .

[5]  S. Pincebourde,et al.  Microclimatic challenges in global change biology , 2013, Global change biology.

[6]  J. Kingsolver,et al.  Ectotherm thermal stress and specialization across altitude and latitude. , 2013, Integrative and comparative biology.

[7]  M. Chelle,et al.  The development of a foliar fungal pathogen does react to leaf temperature! , 2013, The New phytologist.

[8]  Jérôme Casas,et al.  Temporal coincidence of environmental stress events modulates predation rates , 2012 .

[9]  S. Pincebourde,et al.  Climate uncertainty on leaf surfaces: the biophysics of leaf microclimates and their consequences for leaf‐dwelling organisms , 2012 .

[10]  R. Shine,et al.  Hot mothers, cool eggs: Nest-site selection by egg-guarding spiders accommodates conflicting thermal optima , 2012 .

[11]  Chloé Lahondère,et al.  Mosquitoes Cool Down during Blood Feeding to Avoid Overheating , 2012, Current Biology.

[12]  Michael J Angilletta,et al.  The world is not flat: defining relevant thermal landscapes in the context of climate change. , 2011, Integrative and comparative biology.

[13]  Ichiro Terashima,et al.  Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower. , 2011, Plant & cell physiology.

[14]  Christian Körner,et al.  Infra‐red thermometry of alpine landscapes challenges climatic warming projections , 2009 .

[15]  G. Davidowitz,et al.  Insect eggs protected from high temperatures by limited homeothermy of plant leaves , 2009, Journal of Experimental Biology.

[16]  C. Harley,et al.  On the prediction of extreme ecological events , 2009 .

[17]  Michael Kearney,et al.  The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming , 2009, Proceedings of the National Academy of Sciences.

[18]  C. Körner,et al.  Tree species diversity affects canopy leaf temperatures in a mature temperate forest , 2007 .

[19]  Jérôme Casas,et al.  Regional climate modulates the canopy mosaic of favourable and risky microclimates for insects. , 2007, The Journal of animal ecology.

[20]  S. Assmann,et al.  Light regulation of stomatal movement. , 2007, Annual review of plant biology.

[21]  Jérôme Casas,et al.  Herbivory mitigation through increased water-use efficiency in a leaf-mining moth-apple tree relationship. , 2006, Plant, cell & environment.

[22]  E. Maggi,et al.  Temporal variance reverses the impact of high mean intensity of stress in climate change experiments. , 2006, Ecology.

[23]  S. Pincebourde,et al.  MULTITROPHIC BIOPHYSICAL BUDGETS: THERMAL ECOLOGY OF AN INTIMATE HERBIVORE INSECT–PLANT INTERACTION , 2006 .

[24]  Li-zhi Wang,et al.  Effect of thermal acclimation on preferred temperature, avoidance temperature and lethal thermal maximum of Macrobiotus harmsworthi Murray (Tardigrada, Macrobiotidae) , 2005 .

[25]  M. Berenbaum,et al.  Indirect effects of insect herbivory on leaf gas exchange in soybean , 2005 .

[26]  Catherine Massonnet,et al.  Variabilité architecturale et fonctionnelle du système aérien chez le pommier (Malus domestica Borkh.): comparaison de quatre cultivars par une approche de modélisation structure-fonction , 2004 .

[27]  L. D. Talbott,et al.  The guard cell chloroplast: a perspective for the twenty-first century. , 2002, The New phytologist.

[28]  J. Whittaker Insects and plants in a changing atmosphere , 2001 .

[29]  L. Tanigoshi,et al.  Effect of Temperature on Development and Demographic Parameters of Tetranychus urticae and Eotetranychus carpini borealis (Acari: Tetranychidae) , 2001 .

[30]  Hervé Sinoquet,et al.  RATP: a model for simulating the spatial distribution of radiation absorption, transpiration and photosynthesis within canopies: application to an isolated tree crown , 2001 .

[31]  Hong S. He,et al.  An aggregation index (AI) to quantify spatial patterns of landscapes , 2000, Landscape Ecology.

[32]  K. Mott,et al.  Patchy stomatal conductance: emergent collective behaviour of stomata. , 2000, Trends in plant science.

[33]  D. Easterling,et al.  Observed variability and trends in extreme climate events: A brief review , 2000 .

[34]  Nathan Phillips,et al.  Survey and synthesis of intra‐ and interspecific variation in stomatal sensitivity to vapour pressure deficit , 1999 .

[35]  Hamlyn G. Jones,et al.  Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces , 1999 .

[36]  Robertson,et al.  Thermal avoidance during flight in the locust Locusta migratoria , 1996, The Journal of experimental biology.

[37]  John L. Monteith,et al.  A reinterpretation of stomatal responses to humidity , 1995 .

[38]  D. Fournier,et al.  Activité migratoire des tétranyques: Mise en évidence d'un rythme , 1989, Entomophaga.

[39]  E. Southwick,et al.  Microclimates of Small Arthropods: Estimating Humidity within the Leaf Boundary Layer , 1984 .

[40]  C. Field,et al.  Determinants of leaf temperature in California Mimulus species at different altitudes , 1982, Oecologia.

[41]  J. Monteith,et al.  Boundary Layer Climates. , 1979 .

[42]  J. Kingsolver Thermal and Hydric Aspects of Environmental Heterogeneity in the Pitcher Plant Mosquito , 1979 .

[43]  E. Linacre Further notes on a feature of leaf and air temperatures , 1967 .

[44]  A. Leopold,et al.  Transpiration: Its Effects on Plant Leaf Temperature , 1964, Science.

[45]  H. Mori The Effects of Photo-Stimulus on the Thermal Reaction in Four Species of Spider Mites(Acarina Tetranychidae) , 1962 .

[46]  A. Krogh,et al.  The Mechanism of Flight Preparation in Some Insects , 1941 .

[47]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[48]  J. Deneubourg,et al.  Group effect on fertility, survival and silk production in the web spinner Tetranychus urticae (Acari: Tetranychidae) during colony foundation , 2010 .

[49]  M. Angilletta Thermal Adaptation: A Theoretical and Empirical Synthesis , 2009 .

[50]  Steven L. Chown,et al.  Insect physiological ecology : mechanisms and patterns , 2004 .

[51]  J. Bunce Does transpiration control stomatal responses to water vapour pressure deficit , 1997 .

[52]  K. McGarigal,et al.  FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. , 1995 .

[53]  P. Willmer Microclimate and the Environmental Physiology of Insects , 1982 .

[54]  Gaylon S. Campbell,et al.  Biophysical ecology: (Springer Advanced Texts in Life Sciences.) David M. Gates. Springer-Verlag, New York, NY, 1980, xxiii + 611 pp., 163 figs., 30 tabs., DM 79.50, U.S. $43.80 (clothbound). , 1981 .

[55]  G. Campbell,et al.  An Introduction to Environmental Biophysics , 1977 .