J Insect Behav (2013) 26:14–22 DOI 10.1007/s10905-012-9329-5
Signaling or Not-Signaling: Variation in Vulnerability and Defense Tactics of Armored Ground Crickets (Acanthoplus Speiseri: Orthoptera, Tettigoniidae, Hetrodinae) Philip W. Bateman & Patricia A. Fleming
Revised: 9 March 2012 / Accepted: 3 April 2012 / Published online: 26 April 2012 # Springer Science+Business Media, LLC 2012
Abstract Male Orthoptera singing from exposed perches are at risk from acoustically- and visually-hunting predators. The defensive reactions of armored ground crickets (Acanthoplus speiseri) include falling silent, dropping from their perch, alarm stridulation and autohaemorrhaging. Male and female ground crickets show different reactivity (i.e. the number or intensity of defense tactics used) to predation, depending on level of exposure: calling males were more reactive when approached during daylight, compared with in the dark. During daylight, calling males were more reactive than silent, cryptic, males and females. The level of response presumably reflected the riskiness of the individual’s behavior and situation at that time. Plasticity of response to predation allows individuals to balance risky behavior (i.e. acoustic signaling from exposed perches) by being more reactive to potential threats. Keywords Anti-predation response . acoustic communication
Introduction Attracting a mate by signaling visually or acoustically is a risky business because predators may eavesdrop on the cues aimed at the potential mate (Zuk and Kolluru 1998). Calling or displaying individuals that give away their position are therefore more vulnerable to potential predators and parasitoids than the rest of the population (e.g. Burk 1982; Belwood and Morris 1987; Kotiaho et al. 1998; Hedrick 2000). Due to their acoustic signaling, often from exposed positions, calling male Orthoptera can P. W. Bateman (*) Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa e-mail:
[email protected] P. W. Bateman : P. A. Fleming School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia
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become vulnerable to acoustically- and visually-hunting predators (Burk 1982; Zuk and Kolluru 1998). Due to their increased risk of being discovered and captured, we therefore expect that they may have different antipredator behavior to females or nonsignaling males. The threat sensitivity hypothesis (Sih 1986) predicts that prey organisms will assess and adjust their behavior in accordance with the magnitude of the threat from predators. Variation in flexibility of responses to predators has been observed both between and within different taxa depending on such factors as the presence of predators (e.g. varying with predator presence or absence, as well as predator population density), the intensity of predator signals (e.g. olfactory and/or visual predator signals) or predator hunger level (e.g. Sih 1992; Tikkanen et al. 1996; Laurila 2000; Smith and Belk 2001; Lima 2009). Antipredator responses will also vary according to the level of risk that individual prey species are exposed to. For example, there may be differences between individuals according to their intrinsic or temporal vulnerability, with conspicuous males or individuals with low condition and compromised escape ability having greater vulnerability (e.g. Gyssels and Stoks 2005; Lea and Blumstein 2011). For many individuals, potential risk from predation can alter on very short temporal scales if individuals switch between less and more risky behavior. For example, signaling males may switch between signaling for mates visually and/or acoustically and being cryptic and/or silent (Lima and Bednekoff 1999). Animals that have a repertoire of antipredator responses may utilize some or all these tactics when approached or attacked by a predator, or vary these responses in intensity in a state-dependent way based on intrinsic vulnerability to predation (e.g. varying with sex, Loughry and McDonough 1989) or temporal vulnerability to predation (e.g. varying with specific behavior at a particular time, Kotiaho et al. 1998; Lea and Blumstein 2011). Armored ground crickets, Acanthoplus spp. (Orthoptera, Tettigoniidae, Hetrodinae) of southern Africa (locally known as setotojane, koringkrieke, ground crickets or corn crickets) are corpulent, flightless, large (5 cm long) insects with spiny pronota and legs which are well-known throughout their range because of their swarms during the austral autumn which may cause significant damage to crops (Mbata 1992a; Minja et al. 1999). Before swarming is triggered, however, these ground crickets are sedentary, and at this stage of their life cycle adults of both sexes adopt cryptic behavior, foraging singly in low bushes and tall grasses (Mbata 1992b) and moving slowly (behavior likely to increase the effectiveness of crypsis, Hatle and Faragher 1998). Adult males, as is typical for most Orthoptera (see Robinson and Hall 2002 for a review), advertise their presence to potential mates by stridulating (Bateman and Ferguson 2004) producing an uninterrupted buzz similar to that of other Acanthoplus species (P.W.B. pers. obs.; Conti and Viglianisi 2005; Kowalski and Lakes-Harlan 2011). Males may also act as ‘silent seducers’, by perching near stridulating conspecifics and attempting to intercept approaching females, thereby presumably saving energy as well as retaining their crypsis (Mbata 1992b). Their grouping behaviour, large numbers, and range of behaviours in regard to securing mates makes these animals useful to investigate the varying effects of reproductive strategies on predator avoidance. Under laboratory conditions, A. discoidalis displays a wide repertoire of graded antipredator responses in response to either simulated attacks from the side (pinching
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their legs with forceps) or above (gripping their pronota) (Bateman and Fleming 2009). Males produced ‘alarm’ stridulation and both sexes attempted to bite, regurgitate their crop contents (Bateman and Fleming 2009) and autohemorrhage (reflex bleeding: where hemolymph is forcibly ejected from seams in the integument), a behavior common to all Acanthoplus spp. thus far examined (P.W.B. pers. obs.; Bateman and Fleming 2009) as well as other hetrodines (Glenn 1991, Grzeschik 1969). Alarm stridulation appears to be more common in Orthoptera that are slowmoving or cryptic (Heller 1996), supporting the idea that it is a deimatic display, startling a predator. Autohemorrhage may be effective against predators in Acanthoplus spp. (Bateman and Fleming 2009). Regurgitating crop contents can also be an effective defense for various orthopteran species (Lymbery and Bailey 1980; Sword 2001). Importantly, their defensive responses can be tailored to the direction of attack, with attack from the side eliciting biting, more stridulation, regurgitation and projectile autohemorrhaging over greater distances than did attack from above (Bateman and Fleming 2009). The different responses appear to reflect adaptations to modes of attack from different predators. Hetrodines have been seen to be eaten by red-billed and yellow-billed hornbills (Tockus erythrorhynchus, T. leucomelas), and amur falcons (Falco amurensis) (P.W.B. pers.obs.), are presumed to be preyed upon by lesser kestrels (Falco naumanni) (Visagie and Anderson 2006) and have been found in the stomachs of black-backed jackals (Canis mesomelas) and bat-eared foxes (Otocyon megalotis) (Bothma 1966). Flexibility in defense response and the wide repertoire of defense techniques suggests that Acanthoplus spp. can alter their behavior according to degree of potential risk. We investigated the escape and defense tactics of the Zambian armored ground cricket A. speiseri Brancsik in response to simulated predator approach and attack under field conditions. We compared the responses of exposed (calling) males to more cryptic individuals (non-calling males and females) to test the following predictions: i) calling males approached during daylight (i.e. when potentially exposed to acoustically- and visually-hunting predators) would be more likely to respond to the visual presence of a predator than calling males approached at night; ii) calling males will be more sensitive to the perceived threat of a predator than their silent conspecifics, and would subsequently show greater antipredator responses than would silent males and females; iii) but that both calling and silent males and females should both be equally sensitive to being touched, an indication that they had been discovered by the putative predator (in this case, experimenter).
Methods Acanthoplus speiseri is distributed across central Zimbabwe and into Zambia with isolated records from South Africa and Malawi (Irish 1992). Acanthoplus speiseri is similar in size and shape to other Acanthoplus species, except for diagnostic differences in pronotal spination (Irish 1992). During this study in the Zambezi Valley of northern Zimbabwe in May of 2010, the A. speiseri seen were a pale green color
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which, along with immobility or slow movement, may have enhanced their crypsis against green vegetation (e.g. Hatle and Faragher 1998). We located most individuals in Indigofera sp. bushes (90 % of the total of 110 animals) near roads and tracks, where the ground crickets were usually perched just below the apex of the bush between 1 and 1.5 m above ground. Alternative perch sites (10 % of individuals) included grass and forbs. We recorded the earliest calling males from approximately midday; calling increased towards late afternoon and could also be heard for approximately 2 h after dark (18:00). We located and captured 88 individuals in the afternoon (daylight) and 22 individuals in the two hours after dark (aided by dimmed LED head torches). Once we had visually located a calling male by triangulation from about 5 m away, one of us (P.W.B.) approached it at a practiced slow walk, with his right arm outstretched, pointing towards the insect to touch it. The other researcher (P.A.F.) observed from a distance (~5 m) to watch for other individuals in the bush. We recorded: 1. The distance in meters (from the outstretched fingertip to the cricket) at which the male stopped calling; this was recorded as 0 m if the animal did not stop calling until it was touched. Falling silent is a common response in calling orthopterans to the presence of danger (see Zuk and Kolluru 1998). 2. The number of animals that dropped from their perch site to the ground when the observer continued to approach. 3. The distance from fingertip to the cricket where it dropped was recorded; this was recorded as 0 m if the animal did not drop until it was touched. 4. The number of times (maximum 3 times, 1 per second) the animal was touched on its pronotum until it responded by dropping. 5. If the animal did not drop in response to 3 touches, it was picked up by gently pinching it between thumb and forefinger; if it had dropped to the ground it was located and similarly picked up. We held animals in this manner for 30 s, during which time we noted whether it produced alarm stridulation, autohemorrhaged, or regurgitated its crop contents. Although the biological significance of this stridulation has not been tested (Grzeschik 1969), stridulation is clearly a response to being held by the observer (a potential predator) (Bateman and Fleming 2009). We also searched the bushes near the calling male for females and non-calling males. We approached these animals in the same way as described above except that we obviously could not record cessation of calling for silent males and females, or alarm stridulation by females. We cannot preclude that ‘non-calling’ males had simply stopped calling earlier; the contrast between males is therefore between males that continued to call when approached to within 10 m (‘calling’ males) and those that fell silent when the observer was >10 m away (‘non-calling’ males). We analyzed behavioral response data by Pearson’s χ2df analysis for differences between the sexes and time of approach (day vs. night), with expected values for each comparison calculated and assuming that an equal proportion of each cohort showed the behavioral response in question. We compared the distances at which calling males would stop calling and/or drop from their perch, and the number of times that they could be touched, between daylight and night time approaches using non-
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parametric Mann–Whitney U Test. There were insufficient numbers of other cohorts (non-calling males and females) to do similar comparisons. Level of statistical significance was set at α
