Male sexual behavior and pheromone emission is enhanced by exposure to guava fruit volatiles in Anastrepha fraterculus

Authors: BACHMANN, GUILLERMO - Instituto Nacional Tecnologia Agropecuaria; SEGURA, DIEGO - Instituto Nacional Tecnologia Agropecuaria; DEVESCOVI, FRANCISCO - Instituto Nacional Tecnologia Agropecuaria; JUAREZ, M - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); RUIZ, M - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); VERA, M - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); CLADERA, JORGE - Instituto Nacional Tecnologia Agropecuaria; Teal, Peter; FERNANDEZ, PATRICIA - Estacion Experimental Agroindustrial Obispo Colombres (EEAOC)

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/27/2015
Publication Date: 4/29/2015
Citation: Bachmann, G.E., Segura, D.F., Devescovi, F., Juarez, M.L., Ruiz, M.J., Vera, M.T., Cladera, J.L., Teal, P.E., Fernandez, P.C. 2015. Male sexual behavior and pheromone emission is enhanced by exposure to guava fruit volatiles in Anastrepha fraterculus. PLoS One. doi: 10.1371/journal.pone.0124250.

Interpretive Summary: Phytochemicals from host plants are well known to affect behaviour and physiology across a wide range of insect species (Schoonhoven et al., 2005). In several phytophagous insect species, males are attracted to volatile compounds released by the host plant, increasing the probability of encountering females (Thornhill and Alcock, 1983; Bernays and Chapman, 1994). However, host plants offer benefits other than cues to find mating partners, and insects have developed different strategies to optimize mating and reproductive success making use of plant chemicals. In some cases, insects acquire host plant chemicals and use them as pheromones or precursors, in others, this chemicals synergize or otherwise induce or enhance the emission of sex pheromones or the response from the receiver (reviewed in Landolt and Phillip, 1997; Reddy and Guerrero, 2004). Tephritid fruit flies have evolved a wide range of mating systems, and host and non-host plants play an important role in shaping male sexual behaviour and mating success in many ways (Aluja and Norrbom, 2000). Among fruit-ovipositing species, males of species having a narrow host range typically encounter females at oviposition sites as occurs in the apple maggot fly, Rhagoletis pomonella (Walsh). Males of this species rest on host fruits waiting for the females, with which they mate upon arrival (Prokopy et al., 1971). In contrast, in polyphagous Tephritidae fruit flies, female location is less predictable, and males aggregate and release sex pheromone in groups (termed leks) to attract females (Prokopy, 1980; Burk, 1981; Shelly and Kaneshiro, 1991). In some species of Bactrocera, such as the oriental fruit fly, Bactrocera dorsalis (Hendel), males are strongly attracted to methyl eugenol, a natural chemical found in certain species of plants, which is ingested by the males and serves as a precursor in the synthesis of sex pheromone (Shelly and Dewire, 1994; Tan and Nishida, 1996). Males deprived of this precursor produce a less attractive pheromone, which results in a lower mating success (Nishida et al., 1997). Studies on the Queensland fruit fly, Bactrocera Tryoni Froggatt showed an enhancement of mating success in males fed on cuelure and zingerone (Kumaran et al. 2013), and also changes in pheromonal compounds after lure feeding and subsequent enhanced female attraction to modified pheromone moieties of males fed on cuelure (Kumaran et al. 2014a). In the Mediterranean fruit fly Ceratitis capitata (Wiedemann), the exposure of males to host fruit volatiles increases male mating success (Papadopoulos et al., 2001; Shelly, 2001; Shelly and McInnis, 2001; Shelly and Villalobos, 2004; Shelly at el., 2008). Although the mechanisms underlying this phenomenon are less understood than for B. dorsalis, the increase in mating success seems to be related to an increase in male pheromone calling behaviour (Shelly, 2001; Papadopoulos et al., 2006) and also to an alteration in close-range olfactory cues (Shelly et al., 2007b). This phenomenon has recently been explored in the olive fly, Bactrocera oleae (Gmelin), for which the exposure to a-pinene increases mating performance of males and females (Gerofotis et al., 2013). A recent study indicates that laboratory males of the South American fruit fly, Anastrepha fraterculus (Wiedemann), exposed to guava fruit (Psidium guajava L.), one of the preferred hosts of A. fraterculus, mate more frequently than males that have not been exposed to guava (Vera et al., 2013). This is true even when males are exposed only to fruit volatiles and were not allowed to contact the fruit (Vera et al., 2013). The sexual behaviour of A. fraterculus has been analyzed in some Brazilian and Argentinean populations (Malavasi et al., 1983; Petit-Marty et al., 2004; Sciurano et al., 2007; Segura et al., 2007; Gómez Cendra et al., 2011). Mating occurs early in the morning

Technical Abstract: Host plant chemicals can influence sex pheromone communication of tephritid fruit flies, and affect strategies optimizing mating and reproduction. Previous studies suggest that females of the South American fruit fly, Anastrepha fraterculus, prefer to mate with laboratory males previously exposed to guava volatiles. The present study confirms this observation both for laboratory and wild males and investigates the mechanism underlying this phenomenon. Results confirmed previous findings that guava exposure increased male mating competitiveness and revealed that it affects male calling behaviour and pheromone release. This strongly suggests that guava influences male mating competitiveness through an enhancement of chemical and physical signals related to the communication between sexes. Changes in male behaviour, induced by guava exposure, appear to be particularly remarkable during the initial phase of the sexual activity period, when most of the mating pairs are formed. The enhanced mating success was partially reproduced by using a subset of volatile chemicals present in guava fruit, which opens a door for research on the use of sexual competitiveness enhancers for pest control.