Understanding costs and benefits of thermal plasticity for pest management: insights from the integration of laboratory, semi-field and field assessments of Ceratitis capitata (Diptera: Tephritidae).

The relative costs and benefits of thermal acclimation for manipulating field performance of pest insects depend upon a number of factors including which traits are affected and how persistent any trait changes are in different environments. By assessing plastic trait responses of Ceratitis capitata (Mediterranean fruit fly) across three distinct operational environments (laboratory, semi-field, and field), we examined the influence of different thermal acclimation regimes (cool, intermediate [or handling control], and warm) on thermal tolerance traits (chill-coma recovery, heat-knockdown time, critical thermal minimum and critical thermal maximum) and flight performance (mark-release-recapture). Under laboratory conditions, thermal acclimation altered thermal limits in a relatively predictable manner and there was a generally positive effect across all traits assessed, although some traits responded more strongly. By contrast, dispersal-related performance yielded strongly contrasting results depending on the specific operational environment assessed. In semi-field conditions, warm- or cold-acclimated flies were recaptured more often than the control group at cooler ambient conditions suggesting an overall stimulatory influence of thermal variability on low-temperature dispersal. Under field conditions, a different pattern was identified: colder flies were recaptured more in warmer field conditions relative to other treatment groups. This study highlights the trait- and context-specific nature of how thermal acclimation influences traits of thermal performance and tolerance. Consequently, laboratory and semi-field assessments of dispersal may not provide results that extend into the field setting despite the apparent continuum of environmental complexity among them (laboratory < semi-field < field).

A transcriptomics assessment of oxygen-temperature interactions reveals novel candidate genes underlying variation in thermal tolerance and survival.

While single stress responses are fairly well researched, multiple, interactive stress responses are not-despite the obvious importance thereof. Here, using D. melanogaster, we investigated the effects of simultaneous exposures to low O2 (hypoxia) and varying thermal conditions on mortality rates, estimates of thermal tolerance and the transcriptome. We used combinations of 21 (normoxia), 10 or 5kPa O2 with control (23°C), cold (4°C) or hot (31°C) temperature exposures before assaying chill coma recovery time (CCRT) and heat knock down time (HKDT) as measures of cold and heat tolerance respectively. We found that mortality was significantly affected by temperature, oxygen partial pressure (PO2) and the interaction between the two. Cold treatments resulted in low mortality (<5%), regardless of PO2 treatment; while hot treatments resulted in higher mortality (∼20%), especially at 5kPa O2 which was lethal for most flies (∼80%). Both CCRT and HKDT were significantly affected by temperature, but not PO2, of the treatments, and the interaction of temperature and PO2 was non-significant. Hot treatments led to significantly longer CCRT, and shorter HKDT in comparison to cold treatments. Global gene expression profiling provided the first transcriptome level response to the combined stress of PO2 and temperature, showing that stressful treatments resulted in higher mortality and induced transcripts that were associated with protein kinases, catabolic processes (proteases, hydrolases, peptidases) and membrane function. Several genes and pathways that may be responsible for the protective effects of combined PO2 and cold treatments were identified. We found that urate oxidase was upregulated in all three cold treatments, regardless of the PO2. Small heat shock proteins Hsp22 and Hsp23 were upregulated after both 10 and 21kPa O2-hot treatments. Collectively, the data from PO2-hot treatments suggests that hypoxia does exacerbate heat stress, through an as yet unidentified mechanism. Hsp70B and an unannotated transcript (CG6733) were significantly differentially expressed after 5kPa O2-cold and 10kPa O2-hot treatments relative to their controls. Downregulation of these transcripts was correlated with reduced thermal tolerance (longer CCRT and shorter HKDT), suggesting that these genes may be important candidates for future research.

The metabolic costs of sexual signalling in the chirping katydid Plangia graminea (Serville) (Orthoptera: Tettigoniidae) are context dependent: cumulative costs add up fast.

Katydids produce acoustic signals via stridulation, which they use to attract conspecific females for mating. However, direct estimates of the metabolic costs of calling to date have produced diverse cost estimates and are limited to only a handful of insect species. Therefore, in this study, we investigated the metabolic cost of calling in an unstudied sub-Saharan katydid, Plangia graminea Using wild-caught animals, we measured katydid metabolic rate using standard flow-through respirometry while simultaneously recording the number of calls produced. Overall, the metabolic rate during calling in P. graminea males was 60% higher than the resting metabolic rate (0.443±0.056 versus 0.279±0.028 ml CO2 h-1 g-1), although this was highly variable among individuals. Although individual call costs were relatively inexpensive (ranging from 0.02 to 5.4% increase in metabolic rate per call), the individuals with cheaper calls called more often and for longer than those with expensive calls, resulting in the former group having significantly greater cumulative costs over a standard amount of time (9.5 h). However, the metabolic costs of calling are context dependent because the amount of time spent calling greatly influenced these costs in our trials. A power law function described this relationship between cumulative cost (y) and percentage increase per call (x) (y=130.21x-1.068, R2=0.858). The choice of metric employed for estimating energy costs (i.e. how costs are expressed) also affects the outcome and any interpretation of costs of sexual signalling. For example, the absolute, relative and cumulative metabolic costs of calling yielded strongly divergent estimates, and any fitness implications depend on the organism's energy budget and the potential trade-offs in allocation of resources that are made as a direct consequence of increased calling effort.

The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector.

The energetics of processing a meal is crucial for understanding energy budgets of animals in the wild. Given that digestion and its associated costs may be dependent on environmental conditions, it is necessary to obtain a better understanding of these costs under diverse conditions and identify resulting behavioural or physiological trade-offs. This study examines the speed and metabolic costs - in cumulative, absolute and relative energetic terms - of processing a bloodmeal for a major zoonotic disease vector, the tsetse fly Glossina brevipalpis, across a range of ecologically relevant temperatures (25, 30 and 35°C). Respirometry showed that flies used less energy digesting meals faster at higher temperatures but that their starvation tolerance was reduced, supporting the prediction that warmer temperatures are optimal for bloodmeal digestion while cooler temperatures should be preferred for unfed or post-absorptive flies. (13)C-Breath testing revealed that the flies oxidized dietary glucose and amino acids within the first couple of hours of feeding and overall oxidized more dietary nutrients at the cooler temperatures, supporting the premise that warmer digestion temperatures are preferred because they maximize speed and minimize costs. An independent test of these predictions using a thermal gradient confirmed that recently fed flies selected warmer temperatures and then selected cooler temperatures as they became post-absorptive, presumably to maximize starvation resistance. Collectively these results suggest there are at least two thermal optima in a given population at any time and flies switch dynamically between optima throughout feeding cycles.

Fitness costs of rapid cold-hardening in Ceratitis capitata.

Rapid cold-hardening (RCH) is a unique form of phenotypic plasticity which confers survival advantages at low temperature. The fitness costs of RCH are generally poorly elucidated and are important to understanding the evolution of plastic physiology. This study examined whether RCH responses, induced by ecologically relevant diel temperature fluctuations, carry metabolic, survival, or fecundity costs. We predicted that potential costs in RCH would be manifested as differences in metabolic rate, fecundity, or survival in flies which have hardened versus those which have not, or flies that have experienced more RCH events would show greater costs than those which have experienced fewer events. One group of flies cooled to 10°C for 2 h for 11 consecutive days experienced daily RCH (Hardened), whereas the other group exposed to 15°C for the same 2-h period each day formed a Control group. Hardened flies had higher survival at -5°C for 2 h than control flies (69 ± 9% vs. 44 ± 19%, P = 0.04). Hardened flies showed no metabolic or fecundity costs, but had reduced average survival (P = 0.0403). Thus, a major cost to repeated low temperature exposures in Ceratitis capitata is through direct mortality caused by chilling injury, although this appears not to be a direct cost of RCH.

Costs and benefits of thermal acclimation for codling moth, Cydia pomonella (Lepidoptera: Tortricidae): implications for pest control and the sterile insect release programme.

Sterile insect release (SIR) is used to suppress insect pest populations in agro-ecosystems, but its success hinges on the performance of the released insects and prevailing environmental conditions. For example, low temperatures dramatically reduce SIR efficacy in cooler conditions. Here, we report on the costs and benefits of thermal acclimation for laboratory and field responses of codling moth, Cydia pomonella. Using a component of field fitness, we demonstrate that low temperature acclimated laboratory-reared moths are recaptured significantly more (∼2-4×) under cooler conditions in the wild relative to warm-acclimated or control moths. However, improvements in low temperature performance in cold-acclimated moths came at a cost to performance under warmer conditions. At high ambient temperatures, warm-acclimation improved field performance relative to control or cold-acclimated moths. Laboratory assessments of thermal activity and their limits matched the field results, indicating that these laboratory assays may be transferable to field performance. This study demonstrates clear costs and benefits of thermal acclimation on laboratory and field performance and the potential utility of thermal pretreatments for offsetting negative efficacy in SIR programmes under adverse thermal conditions. Consequently, the present work shows that evolutionary principles of phenotypic plasticity can be used to improve field performance and thus possibly enhance pest control programmes seeking increased efficacy.