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Plasticity of the Phonotactic Selectiveness of Four Species of Chirping Crickets (Gryllidae): Implications for Call Recognition Benjamin Navia

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Plasticity of the Phonotactic Selectiveness of Four Species of Chirping Crickets (Gryllidae): Implications for Call Recognition Benjamin Navia Andrews University From the SelectedWorks of Benjamin Navia Winter January 5, 2010 Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition Benjamin Navia Available at: https://works.bepress.com/benjamin-navia/14/ Physiological Entomology (2010) 35, 99–116 DOI: 10.1111/j.1365-3032.2009.00713.x Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition JOHN STOUT1, BENJAMIN NAVIA2, JASON JEFFERY1, LESLIE SAMUEL1, LAURA HARTWIG1, ASHLEY BUTLIN1, MARY CHUNG1, JESSICA WILSON1, ERICA DASHNER1 andGORDON ATKINS1 1Biology Department, Andrews University Berrien Springs, Michigan, U.S.A. and 2Department of Human Biology, Kettering College of Medical Arts, Kettering, Ohio, U.S.A. Abstract. Earlier studies of phonotaxis by female crickets describe this selective behavioural response as being important in the females’ choices of conspecific males, leading to reproduction. In the present study, moderate (30+) to very large data sets of phonotactic behaviour by female Acheta domesticus L., Gryllus bimaculatus DeGeer, Gryllus pennsylvanicus Burmeister and Gryllus veletis Alexander demonstrate substantially greater plasticity in the behavioural choices, as made by females of each species, for the syllable periods (SP) of model calling songs (CS) than has been previously described. Phonotactic choices by each species range from the very selective (i.e. responding to only one or two SPs) to very unselective (i.e. responding to all SPs presented). Some females that do not respond to all SPs prefer a range that includes either the longest or shortest SP tested, which fall outside the range of SPs produced by conspecific males. Old female A. domesticus and G. pennsylvanicus are more likely to be unselective for SPs than are young females. Each species includes females that do not respond to a particular SP when responding to CSs with longer and shorter SPs. The results suggest that the plasticity of phonotactic behaviour collectively exhibited by the females of each species does not ensure that choices of a male’s CS effectively focus the female’s phonotactic responses on CSs that represent the conspecific male. The phonotactic behaviour collectively exhibited by females of each species does not readily fit any of the models for selective processing by central auditory neurones that have been proposed to underlie phonotactic choice. Key words. Call recognition, L3/AN2 neurone, neuronal filtering, phonotaxis, plasticity, selective behaviour. Introduction several species and has been described as a rather consis- tent, species-specific behaviour that precedes mating (Popov Female crickets locate and walk towards (phonotactic behav- & Shuvalov, 1977; Moiseff et al., 1978; Pollack & Hoy, 1981; iour) the source of model calling songs (CSs) when their Thorson et al., 1982; Doherty, 1985a; Stout & McGhee, 1988). carrier frequencies (4–5 kHz) and their temporal structures In many species, syllable period (SP) is the most important are similar to that produced in the CSs of conspecific males temporal feature of the CS used by females to discriminate (Popov & Shuvalov, 1977; Stout et al., 1983; Jeffery et al., between calls of males of different species. Thorson et al. 2005). Phonotaxis by female crickets has been examined in (1982) report that female Gryllus campestris respond with SP- selective phonotaxis to CSs with SPs in the range 40–60 ms, Correspondence: John Stout, Biology Department, Andrews Uni- which is characteristic of the CS of conspecific males. Jeffery versity Berrien Springs, Michigan 49104, U.S.A. Tel.: +1 269 471 et al. (2005) demonstrate that female G. pennsylvanicus are 3261; fax: +1 269 471 6911; e-mail: [email protected] most attracted to CSs with SPs in the range 35–60 ms. Female © 2010 The Authors Journal compilation © 2010 The Royal Entomological Society 99 100 J. Stout et al. G. bimaculatus (Doherty, 1985a) show an attractive range of Louisiana). The crickets were raised to adults in 40-L plastic SPs similar to that reported for G. campestris and exhibit little containers under an LD 12 : 12 h photoperiod (lights on ◦ variability that can be attributed to the order of presentation of 06.00 h) at 21–22 C. Cricket chow (Fluker’s Cricket Farm), the stimuli. water, and egg cartons (for shelter) were provided in each In an early comparative study of phonotactic responses of container. Each day, the containers were checked for adults. female crickets to the CS of conspecific males, Popov & Newly-moulted females (0 days old) were isolated from the Shuvalov (1977) first suggest plasticity in the phonotactic males each day and transferred to 16-L containers, containing responses of female crickets from five different species. The paper towels for cover, and were housed in a separate study concludes that the phonotactic response of females is environmental chamber. Adult males were discarded. Cricket not a fixed, automatic reaction but a rather complex behaviour chow and water were provided daily. that can be modified by internal and external conditions. In a more recent study, Stout et al. (2007) show that phonotaxis by female G. bimaculatus is variable; some females respond Gryllus pennsylvanicus and G. veletis. Nymphs of these selectively to a range of SPs that included the conspecific species were caught in the field in Berrien and Crawford male’s CS, whereas others are much less selective. counties in Michigan, placed in 16-L containers as nymphs Phonotaxis in female Acheta domesticus is also originally and transferred to 1-L containers on the day of the imaginal described as a rather consistent behaviour: female A. domesti- molt. Otherwise, they were cared for in the laboratory cus are most attracted to CSs with syllable periods in the range using procedures that were identical to those described for 50–70 ms, comprising the range of SPs of the natural CS of A. domesticus. this species (Stout et al., 1983). However, a degree of plastic- ity is described by Walikonis et al. (1991), who demonstrate Gryllus bimaculatus. All experiments were performed at that, as virgin females age, they became less selective for SP the Department of Neurobiology, Institute of Zoology, Univer- (i.e. exhibit phonotaxis to most or all SPs tested). Gray (1999) sity of Goettingen, using their culture of this species. Methods confirms the age-related change in phonotactic selectiveness for caring for this species were very similar to those used in our by this species. Walikonis et al. (1991) also demonstrate that facility, described above. Temperatures were approximately ◦ during periods of maximal juvenile hormone III (JHIII) produc- 25 C under an LD 12 : 12 h photoperiod. Nymphs were raised tion, younger females are most selective to SP, whereas during from eggs in containers (60 × 40 × 40 cm). Adult females periods of lower production of JHIII, older females are unse- were isolated each day from the rest of the colony on the day of lective. The addition of JHIII causes females that are attracted their imaginal molt and placed together in smaller containers. to a broad range of SPs to become as selective for SP as young females (Walikonis et al., 1991; Atkins et al., 2008a). Ongoing studies of the mechanisms that control phonotactic Behavioural testing selectiveness and the underlying bases for recognition of con- specific CSs include extensive work with female A. domesticus Sound stimuli. Computer-generated model calling songs as well as recent studies of the phonotactic behaviour and pro- (5 kHz carrier frequency) were produced with either three cessing by auditory interneurones in female G. pennsylvanicus syllables with a chirp period of 667 ms (A. domesticus)or (Jeffery et al., 2005) and female G. bimaculatus (Jeffery, 2003; 450 ms (G. veletis) or four syllables and a chirp period Stout et al., 2007). Work also has been initiated with female of 500 ms (G. pennsylvanicus, G. bimaculatus), which were G. veletis (Stout et al., 2004). As part of these studies, phono- within the natural range of the conspecific male’s CSs taxis is tested repeatedly, using a standard protocol as a basis (Desutter-Grancolas & Robillard, 2003). The intensity, syllable for additional tests resulting in data sets that range from very duration (20 or 25 ms; 5 ms rise and fall times) and syllable large (500+ experiments) for A. domesticus to moderate (e.g. period (25–90 ms) could be varied. Model CSs were made 30+ experiments for female G. pennsylvanicus).Thesizeof using SoundEdit 16, version 2 (Adobe Corp., San Jose, the data sets for each of the four species allows an evalua- California), generated using an Apple computer (Macintosh tion of both the individuality and plasticity that underlies the Performa 6110; Apple Corp., Cupertino, California) and played many different behavioural choices by females of each species through an amplifier (Technics VC- 4; Panasonic Corp., during phonotaxis. They also provide an important resource Secaucus, New Jersey) and loud speaker (model 40–1221; for evaluating proposed mechanisms for call recognition and Radio Shack, Fort Worth, Texas). CSs were presented in a the underlying plasticity and characteristics that recognition standard nonsequential order with SPs in the range 30–90 ms mechanisms should demonstrate. or 25–90 ms (50, 90, 70, 40, 60, 30 and 80 ms SPs for A. domesticus females and 40, 70, 25, 50, 90, 35, 60, 80 for G. bimaculatus females). Because some G. bimaculatus and G. Materials and methods pennsylvanicus females responded preferentially to CSs with 35 or 40 ms SP and discriminated between CSs with SPs of 35 Animal care and 40 ms, and because the male’s call used syllable durations in the range 20–25 ms (Doherty, 1985a), CSs with SPs of 25, Acheta domesticus. Four-week-old nymphal A. domesticus 35, 40, 50, 60, 70, 80 and 90 ms and a syllable duration of were purchased from Flukers’ Cricket Farm (Baton Rouge, 20 ms were used for these two species.
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