Could Behaviour and Not Physiological Thermal Tolerance Determine Winter Survival of Aphids in Cereal Fields?

December Could Behaviour and Not Physiological Thermal Tolerance Determine Winter Survival of Aphids in Cereal Fields? Lucy Alford * 0 1 2 3 Thiago Oliveira Andrade 0 1 2 3 Romain Georges 0 1 2 3 Franc oise Burel 0 1 2 3 Joan van Baaren 0 1 2 3 0 Competing Interests: The authors have declared that no competing interests exist 1 Funding: This work was funded by a Marie Curie Intra-European Fellowship (FP7-PEOPLE-2010- IEF-326943) awarded to L Alford, F Burel and J van Baaren. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 2 Editor: Robert Glinwood, Swedish University of Agricultural Sciences , Sweden 3 UMR 6553 ECOBIO, Universite de Rennes I , Rennes Cedex , France Traits of physiological thermotolerance are commonly measured in the laboratory as predictors of the field success of ectotherms at unfavourable temperatures (e.g. during harsh winters, heatwaves, or under conditions of predicted global warming). Due to being more complicated to measure, behavioural thermoregulation is less commonly studied, although both physiology and behaviour interact to explain the survival of ectotherms. The aphids Metopolophium dirhodum, Rhopalosiphum padi and Sitobion avenae are commercially important pests of temperate cereal crops. Although coexisting, these species markedly differ in winter success, with R. padi being the most abundant species during cold winters, followed by S. avenae and lastly M. dirhodum. To better understand the thermal physiology and behavioural factors contributing to differential winter success, the lethal temperature (physiological thermotolerance) and the behaviour of aphids in a declining temperature regime (behavioural thermotolerance) of these three species were investigated. Physiological thermotolerance significantly differed between the three species, with R. padi consistently the least cold tolerant and S. avenae the most cold tolerant. However, although the least cold tolerant of the study species, significantly more R. padi remained attached to the host plant at extreme sub-zero temperatures than S. avenae and M. dirhodum. Given the success of anholocyclic R. padi in harsh winters compared to its anholocyclic counterparts, this study illustrates that behavioural differences could be more important than physiological thermotolerance in explaining resistance to extreme temperatures. Furthermore it highlights that there is a danger to studying physiological thermotolerance in isolation when ascertaining risks of ectotherm invasions, the establishment potential of exotic species in glasshouses, or predicting species impacts under climate change scenarios. - Due to a limited ability to regulate body temperature above or below ambient, ectotherms are greatly affected by environmental thermal conditions. The survival of ectotherms at unfavourable thermal conditions is governed by their intrinsic physiological thermotolerance, which can be enhanced by behavioural responses. Subsequently, the physiological thermotolerance of ectotherms has received much research attention with laboratory based measures of intrinsic thermal tolerance e.g. lethal temperature [14], lethal time [5, 6], and supercooling point [710], commonly used as predictors of the field success of ectotherms at unfavourable temperatures (e.g. during harsh winters, heatwaves, or under conditions of predicted global warming) [11]. However, although a strong link between extreme temperatures and ectotherm survival exists, the relationship between temperature lethality and survival in the field has often yet to be empirically established [2]. Furthermore, when subjected to increasingly low or high temperatures, a suite of behavioural and physiological responses first take place before the point of temperature induced lethality is reached [12], with detrimental effects to fitness occurring as soon as temperatures are reached that impede movement in search of food, a mate, or in escape of predators [13, 14]. As such, the use of non-lethal behavioural thresholds [15], for example, locomotor thresholds [2, 14, 16, 17], critical temperatures [11, 1822], chill coma temperatures [12;2325] and chill coma recovery [2628] may be of more importance as they provide more ecologically relevant information [27]. Consequently, such measures have received increased research attention in recent years, particularly within the field of insect thermal biology in regard to enhancing knowledge on the consequences of predicted climate change on insect fitness, abundance and distribution, and the implications for pest control [11, 14, 16, 23, 2931]. While the employment of behavioural measures has undoubtedly increased, much to the benefit of our understanding of the impacts of temperature on ectotherms, measures of thermotolerance are commonly performed under laboratory conditions with little relation to the natural environment of the study species. Consequently, such studies therefore provide little information as to how the species may interact with its environment as a form of behavioural thermoregulation to enhance thermal tolerance or survival at extreme temperatures. With recent research suggesting that ectotherms may not have the physiological thermal safety margins as previously thought, ectotherms will be forced to rely increasingly on behavioural thermoregulation in the face of climate change to avoid and survive unfavourable thermal conditions [32]. As such, there is increasing need for investigation into behavioural thermoregulation, in conjunction with physiological thermal tolerance studies, to fully understand the vulnerability of ectotherms to a changing climate and extreme weather events. The present study aims to combine measures of physiological thermotolerance with behavioural thermotolerance to better understand low temperature survival, employing aphids as a model. Aphids are pests to many commercially important crops [33, 34]. During winter months, to maximise survival, aphids commonly overwinter as an egg (holocyclic); the most cold tolerant stage of the aphid life cycle [35]. However, where winter conditions permit, in particular in Western Europe, overwintering may occur as anholocyclic individuals which remain active on host plants [36]. It is this ability to continue reproducing during mild winters which greatly increases the potential for aphid population growth, and in turn the potential for, and severity of, spring pest outbreaks [3740]. Given their importance as pest species, much research has therefore focused on the thermal tolerance of aphids to enhance understanding of population dynamics, pest outbreaks, and, in turn, to better inform biological control practices [2, 3, 14, 41 46]. The focus aphid species of the current study, Metopolophium dirhodum (Walker), Rhopalosiphum padi (Linnaeus) and Sitobion avenae (Fabricius) are three major pests of commercially important cereal crops throughout temp (...truncated)