The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus oligospilus

Abstract

After an insect herbivore has reached its host plant, contact cues from the leaf surface often determine host acceptance. We studied contact cues during oviposition behavior of a willow pest, the sawfly Nematus oligospilus (Hymenoptera: Tenthredinidae), a specialist feeder on Salix (Salicaceae) trees, and how it determines oviposition preference in lab and field conditions. We described the sequence of behaviors that lead to egg laying on the most and least preferred willow species. Then we studied the morphology of chemosensory structures present on the female antenna, cerci and ovipositor. Since phenolic glycosides (PGs) are the main secondary metabolites present in Salicaceae species, we investigated their role in host acceptance. We quantified these compounds in different willow species and correlated PG content with oviposition preference under lab and natural field conditions. We demonstrated a major role for contact cues in triggering N. oligospilus egg laying on the leaf surface of preferred willow genotypes. Firstly cues are sensed by antennae, determining to leave or stay on the leaf. After that, sensing is performed by abdominal cerci, which finally triggers egg laying. The lack of PGs in non-preferred species and the significant correlation observed between PGs, natural damage and oviposition preference suggest a role for these compounds in host selection. Our study suggests that in specialist feeders, secondary compounds normally acting as defenses can actually act as a susceptibility factor by triggering specific insect behavior for oviposition. These defensive compounds could be selected against to increase resistance.

Previous herbivory alerts conspecific gravid sawflies to avoid unsuitable host plants

“…For the remaining types of behaviours, there were no significant differences between treatments (table 2). Since it was suggested that contact chemosensilla from female cercus may play a key role in triggering EG (Fernández et al ., 2019), the frequency of the different types of behaviours performed before and after abdomen rubbing (AR) were analysed. Before AR, females performed the same types of behaviours at the same frequency in UP and DP (χ 2 = 2.39, P = 0.496; fig.…”

“…Moreover, the significant change in the behaviour of the female after contacting the leaf surface strongly suggests the use of contact cues as the last step of decision making during the oviposition process as proposed by Fernández et al . (2019). These results are also in agreement with our previous studies (Braccini et al ., 2013, 2015) reinforcing the idea that orientation of N. oligospilus females on Salix spp.…”

“…Once the female was released in the centre of the device, we observed its behaviour during 60 min and identified which of the six behavioural units described by Fernández et al . (2019) (table 1) was being performed on a given plant. We used a stopwatch to register the duration of each behaviour unit.…”

“…We thus, evaluated neonate hatching, larval performance and survival of larvae that were born and bred on either damaged or undamaged plants. The experimental approach followed is original and differs from all previous research conducted in this system, in which the oviposition substrate offered consisted of several host genotypes with different degrees of constitutive resistance against sawflies (Braccini et al ., 2013; Fernández et al ., 2019). Thus, we studied a novel aspect of the willow tree–sawfly interaction by including the role of the previous herbivory, with special focus on induced defences, on host selection.…”

Host plant genetic control of associated fungal and insect species in a Populus hybrid cross

“…Host selection for oviposition is initially driven by visual cues and reinforced by females assessing the nutrition and chemical cues of foliage (Boeckler, Gershenzon, & Unsicker, 2011; Panda & Khush, 1995). Previous research in Salix (closely related to Populus ) has shown that common phenolic glycosides in leaf tissue are important in host choice in both the free‐feeding Nematus oligospilus and galling Euura amerinae specialist sawflies (Fernández et al, 2019; Kolehmainen, Roininen, Julkunen‐Tiitto, & Tahvanainen, 1994). We therefore pursued QTL mapping of metabolites to determine whether phenolic compounds might be important determinants of the potential ovipositional relationship.…”