3 Mating Behavior of the Asian Citrus Psyllid

3 Mating Behavior of the Asian Citrus Psyllid Richard W. Mankin1* and Barukh Rohde2 1US Department of Agriculture, Agricultural Research Service, Center for Medical, Agricultural, and Veterinary Entomology, Gainesville, Florida, USA; 2Department of Electrical and Computer Engineering, University of Florida, Gainesville, Florida, USA Many aspects of the mating behavior of Diapho- produce signals ranging approximately 150– rina citri Kuwayama (Hemiptera: Liviidae), the 500 ms in duration, and females 331–680 ms. Asian citrus psyllid (ACP) are shared by other mem- The spectra of communication signals produced bers of the Psylloidea. Adults are reproductively by D. citri have prominent frequencies that are mature within about 2 days post-eclosion, and multiples (harmonics) of the 170–250 Hz wing- both sexes mate multiple times during their lifetime. beat frequency, and both sexes respond behav- Typically, courtship is mediated by short-range, iorally to synthetic signals containing three or substrate- borne vibrational communication and more wingbeat harmonics. When the male semiochemicals. In citrus orchards, D. citri court- finds the female, he moves alongside with their ship is facilitated by host-seeking and foraging heads pointing in the same direction and grasps behavior, as both sexes are attracted to green and her with his adjacent legs, bringing his abdo- yellow colors, as well as to volatiles of young men from underneath to meet the opening of flush shoots on the host tree, and short-range her genital segment. They remain in copulation communication is sufficient for finding mates in for about 48 min. Dispersal and mating behavior aggregations that develop soon after the flush of D. citri is influenced by abiotic factors includ- opens. Courtship behavior includes a series of ing light, temperature, storms and barometric duets, in which a searching male produces vi- pressure, and by biotic factors including host brational calls that elicit rapid replies from recep- plant flush, host plant structure, aggregation tive females, enabling him to focus on willing behaviors and learning behaviors. Opportun- partners. Both sexes produce vibrational com- ities exist to co-opt D. citri mating behavior for munication signals by extending and fanning purposes of detecting and managing popula- their wings while their legs hold on to the plant. tions, enabling reductions in the incidence and The signal is transmitted to the host plant struc- spread of the bacteria causing huanglongbing, tures and then detected by vibration- sensitive, a devastating disease of citrus. This chapter chordotonal organs in the legs of the receiving describes details of what is currently known conspecific. During the duetting bouts, male about D. citri mating behavior and how such D. citri call intermittently, with an interval of 9 knowledge has been applied in development of ± 1.4 s (mean ± standard error) between calls, methods that apply vibrational communication and females reply within 0.95 ± 0.09 s. Males to disrupt mating or trap males. * Email: [email protected] © CAB International 2020. Asian Citrus Psyllid: Biology, Ecology and Management 30 of the Huanglongbing Vector (eds. J.A. Qureshi and P.A. Stansly) Mating Behavior of the Asian Citrus Psyllid 31 3.1 Introduction (Burckhardt and Ouvrard, 2012; Martoni et al., 2017), share numerous aspects of reproductive Diaphorina citri Kuwayama (Hemiptera: Liviidae) biology and mating behavior (Lubanga et al., native to India (Hollis, 1987), initially was re- 2014, 2016a). Psylloids reproduce only sexu- ported as a significant psylloid pest of Citrus spp. ally, unlike some hemipterans (Kennedy and in China, Taiwan, Japan and the Philippines in Stroyan, 1959). Many male psylloids reach re- the early 20th century (Crawford, 1912); how- productive maturity within about 2 days post- ever, little was reported about its ecology, life eclosion, and both sexes mate several times (Burts cycle and mating behavior (Husain and Nath, and Fischer, 1967; Van den Berg et al., 1991; 1927; Catling, 1970; Pande, 1971) until it be- Wenninger and Hall, 2007; Guédot et al., 2012; came important as a worldwide vector of huan- Lubanga et al., 2018) during a typical lifetime of glongbing (HLB), a devastating bacterial disease 49 days or longer (Wenninger and Hall, 2008). in citrus orchards (Halbert and Manjunath, Refractory periods have been reported for fe- 2004; Gottwald et al., 2007). The bacterium males of some psyllid species (Lubanga et al., Candidatus Liberibacter spp. (Alphaproteobacte- 2016a) but have not been reported in D. citri. ria) resides in symbiotic bacteriomes within the Newly emerged D. citri females have immature D. citri hemocoel that also contain nutritional and ovaries that remain without mature eggs until defensive symbionts in mutually indispensable as- mating occurs (Dossi and Cônsoli, 2010). Mat- sociations, all of which are transmitted transovari- ing stimulates vitellogenesis and rapid develop- ally (Dan et al., 2017). Economic damage caused ment of oocytes, and females often begin laying by HLB has stimulated interest in development of eggs on the day of mating (Wenninger and Hall, knowledge about D. citri biology and mating be- 2007). Because oocyte maturation is metachro- havior that could be used for an integrated, nous, with only one oocyte developing per oo- multidisciplinary approach to management of genic cycle, the stimulatory effects of mating D. citri and thereby HLB (Aubert, 1990; Grafton- (Dossi and Cônsoli, 2010) may contribute to the Cardwell et al., 2013; Hall et al., 2013), as has polyandry (Wenninger and Hall, 2008) ob- occurred also with other economically important served in this species. General aspects of several insect pests (Mankin, 2012; Benelli et al., 2014; different male reproductive systems in the Psyl- Takanashi et al., 2019). In this chapter, we focus loidea are described in Schlee (1969), Machar- on aspects of mating behavior that can be co-opted ashvili and Kuznetsova (1997) and Kuznetsova to reduce D. citri populations in citrus and other et al. (1997); and the male D. citri genitalia and hosts in the Aurantioideae subfamily of Rutaceae reproductive system were described in Stockton (Halbert and Manjunath, 2004; Hall et al., 2017). et al. (2017b) and Alba-Alejandre et al. (2018). The life stages of D. citri on rough lemon Citrus Dossi and Cônsoli (2014) and Stockton et al. jambhiri Lush, sour orange C. aurantium L., grape- (2017b) described the D. citri female reproduct- fruit C. paradisi Macfadyen, and orange jessamine ive organs. Murraya paniculata (L.) Jack were described by Short-range semiochemicals have been Tsai and Liu (2000). These and other host species demonstrated to play a role in mate-finding of have a range of different physical and structural several (Wenninger et al., 2008; Brown et al., characteristics that, as discussed further below, 2009; Guédot et al., 2009, 2010; Mann et al., strongly affect vibrational signal amplitudes and 2013) but not all psylloids (Lubanga et al., 2016b). the efficacy of mate-seeking behaviors (Cocroft Wu et al. (2016) investigated the antennal and et al., 2006; Mankin et al., 2018). abdominal transcriptomes of male and female D. citri to consider whether chemosensory pro- teins could be identified for development of at- tractants or repellents. It was found that a large 3.2 General Aspects of Mating proportion of chemosensory genes were similar Behavior in Diaphorina citri and Other in male and female antennae and terminal Psylloids abdominal tissues, but two were expressed at higher levels in male than female antennae (Wu Members of the Psylloidea, a group of about et al., 2016), which is consistent with a poten- 3850 phloem-feeding Sternorrhynchan species tial role of antennal chemosensilla in D. citri 32 R.W. Mankin and B. Rohde mate-finding or species identification (Onagbola small insects can stretch their legs between et al., 2008). branches at bifurcations, thereby increasing the In addition, substrate-borne vibrational time delay, which could provide directional cues communication is an important mechanism for at bifurcation points. Nevertheless, background mate location in many psylloids (Ossiannilsson, noise from wind or other loud sound or vibration 1950; Virant-Doberlet and Cokl,̌ 2004; Tishech- sources masks the weak signals produced by kin, 2005; Percy et al., 2006; Lubanga et al., small insects and interferes with precise identifica- 2014, 2016b; Eben et al., 2015; Liao and Yang, tion of the direction of a replying female psyllid 2015, 2017; Liao et al., 2016), as well as other (Tishechkin, 2013). To accommodate directional Hemiptera (Cocroft and Rodríguez, 2005) in- uncertainties and signal masking, many hemip- cluding the Auchenorrhyncha (Percy and Day, terans augment their searching behavior with a 2005) and the Cicadellidae (Gordon et al., ‘call-fly’ strategy under which a searching male 2017). The capability to detect and produce vi- produces substrate-borne vibrational calls spon- brations is essentially ubiquitous in terrestrial taneously when it first lands on a host plant and invertebrates, which attests to the importance of then moves upward and/or towards a receptive vibrational cues for reproduction and predator female who has produced a duetting reply in re- avoidance (Cocroft and Rodríguez, 2005; Pol- sponse to his call (Hunt and Nault, 1991). Such lack, 2017; Takanashi et al., 2019). In many a strategy is beneficial when the females aggre- Hemiptera, sexual communication involves

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