When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest

Abstract

Phytophagous insects evolving in agroecosystems express numerous defences when faced with myriads of natural enemies. Such defensive traits might impair the effectiveness of biological control relying on these natural enemies, mostly parasitoids. In the case of parasitoid threat, these defences consist of the avoidance of the parasitoid (reduced exposure to antagonists through shortening of developmental time), hindrance of oviposition (evasive behaviours and morphological protection) or destruction of the parasitoid eggs (encapsulation and melanisation by means of the immune system). Previous works focused on one defensive trait only when investigating the effects of temperature on host resistance. By doing so, they assumed that all defensive traits would respond uniformly to a change occurring in thermal environment, which remains an undocumented fact. To test this assumption in the context of global warming, we adopted a global overview of host resistance by examining the effects of rising temperatures on multiple defensive traits used by the grape pest, Lobesia botrana, against its larval parasitoids. Although warmer conditions led to reduced exposure to parasitoids by accelerating larval development, warmer conditions also elicited extensive weakening of behavioural and immune defences. These results confirm that temperatures might differently modulate the levels of expression of several defensive traits. An increase in growth rate and pupal mass also occurred, especially for females, which may contribute to greater pest fecundity in the future. However, the decline of L. botrana resistance might enhance the efficiency of the biological control naturally exerted by parasitoids in vineyards, thereby limiting the damage to crops.