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Disentangling landscape and climate effects on insect communities to inform engineering solutions to enhance biological control in a changing climate

Final Report Summary - CLIMLAND (Disentangling landscape and climate effects on insect communities to inform engineering solutions to enhance biological control in a changing climate)

The earth is presently experiencing rapid changes in both climatic conditions and landscape structure. Over the past century the climate has warmed by approximately 0.6°C and the incidence of extreme climatic events such as droughts and heat and cold waves has increased. In addition to climatic changes, much of Europe has experienced large scale intensification over the past 50 years. This intensification has led to a considerable increase in agricultural productivity but also to a simplification of agricultural landscapes, a loss of biodiversity and a degradation of ecosystem services. The current research aimed to investigate and separate the effects of climatic conditions and landscape intensification on a major agricultural pest insect, the cereal aphids (Sitobion avenae, Metopolophium dirhodum, Rhopalosiphum padi) and their natural biological control agents: the carabid beetles (e.g. Pterostichus melanarius, Poecilus cupreus and Pseudoophonus rufipes) and the parasitoid wasps (Aphidius rhopalosiphi, Aphidius avenae, Aphidius matricariae and Aphidius ervi). Using the Long-Term Ecological Research site, Armorique, in Brittany, France, a landscape gradient was determined which ranged from natural ‘bocage’ landscapes to highly intensified landscapes. Sampling fields were selected in each landscape type from which insects were sampled twice per year (Autumn/Winter and Spring/Summer) and returned to the laboratory and housed at 20°C. A series of experiments were conducted to investigate physiological thermotolerance and behavioural thermoregulation of the study insects.

The thermal tolerance of sampled insects was determined using two main protocols. Firstly, the non-lethal thresholds of critical thermal minima (CTmin) and chill coma were measured using a double-walled glass cyclinder protocol as described in Powell & Bale (2006). Secondly, the lethal threshold of lethal temperature (LT50) was determined using a direct-plunge method as described in Sinclair & Chown (2006). Results showed that landscape type did not significantly affect the thermal tolerance of carabid beetles. Carabids are highly mobile species and capable of utilizing a large array of micro-habitats to evade climatic conditions. As a result, carabids could be less tightly linked to, and affected by, local landscape ecology.

However, for the parasitoid wasps and cereal aphid, landscape significantly affected thermal tolerance. For the parasitoid wasps, parasitoids originating from intensively farmed landscapes were the most thermal tolerant and those originating from natural landscapes were the least thermal tolerant. Since parasitoids develop within a dead aphid host fixed to a plant, they are immobile during larval development and thus incapable of evading climatic conditions. As such, parasitoids would be expected to rely more on physiological thermal tolerance to evade unfavourable climatic conditions, since behavioural thermoregulation is limited during development. Consequently, parasitoids should be more tightly linked to, and affected by, local landscape ecology, as supported by the results. Furthermore, more natural habitats provide a greater array of thermal refuges, whilst intensive landscapes provide a more uniform landscape, offering less variety in thermal refuges. As such, insects in intensive landscapes may be unable to engage in behavioural thermoregulation, instead relying on physiological thermotolerance to avoid and survive unfavourable temperature spells. It is also possible that intensive landscapes could select for parasitoids of greater thermal tolerance.

Interestingly, aphids displayed a reverse pattern to that of the parasitoid wasps, with individuals originating from natural landscapes being the most thermal tolerant. As with parasitoid wasps, aphids are restricted to a host and therefore possess a limited mobility to evade unfavourable thermal conditions. Consequently, aphids must adapt to the stressful thermal conditions they encounter. To better explain the contrasting pattern observed for parasitoids and aphids, meteorological measurements were taken along the landscape gradient. Natural landscapes were shown to have colder mean temperatures, although were more buffered from temperature variations, whereas intensive landscapes had warmer mean temperatures, although greater temperature extremes. For aphids, any movement on or away from the host plant to avoid unfavourable temperatures would result in a disruption or cessation of feeding. As such, an aphid would be expected to adapt to the most stressful environment. It is possible that aphids could be more susceptible to mean daily temperatures, although this requires further investigation.

Results on physiological thermotolerance suggest a complex relationship between landscape intensification and insect thermal biology. Recent research has suggested that ectotherms do not possess a physiological thermal safety margin as once thought (Sunday et al., 2014). In the face of global climate change, insects could therefore be forced to rely increasingly on behavioural thermoregulation. This in turn could put increasing pressure on insects in stressful landscapes and on insects restricted by a host species.

In addition to physiological thermotolerance, the potential for behavioural thermoregulation was investigated to determine how insects utilize their environment as a form of behavioural thermoregulation. This led to the development of a specialised observation arena for use with carabid beetle, which could be heated or cooled at a set rate via connection to a programmable alcohol bath. Within the arena, numerous microhabitats were created to enable monitoring of how carabids utilise the microhabitats when under thermal stress. Unfortunately, results proved inconclusive for the carabid beetles and further investigation is required.

Results on aphid behavioural thermoregulation revealed that the aphid species Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi displayed significantly different patterns of drop-off escape behaviour. This was particularly interesting since patterns of drop-off revealed a reverse pattern to that observed for physiological thermotolerance. It was revealed that S. avenae, the species with the greatest physiological thermal tolerance, dropped from a surface at temperatures higher than its counterparts, with 70% of individuals having dropped off before 0°C was reached. Conversely, R. padi, the least cold tolerant species, remained attached at temperatures significantly lower than S. avenae and M. dirhodum. For R. padi, 70% of aphid drop-off occurred after temperatures of -4°C were reached. These findings illustrate the limitations to studying physiological thermotolerance in isolation under laboratory conditions. Based solely on physiological thermotolerance, it would be incorrectly concluded that R. padi is the least adapted to cold conditions of the cereal aphids. Instead, recorded field abundances of cereal aphids in winter confirm the converse (Krespi et al., 1997). However, investigation into behavioural thermoregulation revealed variations that could instead contribute to differential winter survival. The inclusion of behavioural thermoregulation traits into studies of insect thermotolerance has the potential to greatly enhance our understanding of insect, and indeed ectotherm, survival at extreme temperatures, particularly in temperate climates where lower lethal limits are rarely reached and may subsequently play little role in shaping winter populations. These findings highlight the dangers to studying physiological thermotolerance in isolation, especially when establishing risks of ectotherm invasions and establishment potential of exotic species in glasshouses.

Krespi, L., Dedryver, C.A. Creach, V., Rabasse, J.M. Le Ralec, A. & Nénon, J.P. (1997) Variability in the development of cereal aphid parasitoids and hyperparasitoids in oceanic regions as a response to climate and abundance of hosts. Environ Entomol 26: 545-551.

Powell, S.J. & Bale, J.S. (2006) Effect of long-term and rapid cold hardening on the cold torpor temperature of an aphid. Physiological Entomology, 31, 348-352.

Sinclair, B.J. & Chown, S.L. (2006) Rapid cold-hardening in a Karoo beetle, Afrinus sp. Physiological Entomology, 31, 98-101.

Sunday, J.M. Bates, A.E. Kearney, M.R. Colwell, R.K. Dulvy, N.K. Longino, J.T. & Huey, R.B. (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. PNAS doi: 10.1073/pnas.1316145111