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The Foraging Behavior of Lysiphlebus Fabarum (Marshall), a Thelytokous Parasitoid of the Black Bean Aphid in Iran

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The Foraging Behavior of Lysiphlebus Fabarum (Marshall), a Thelytokous Parasitoid of the Black Bean Aphid in Iran J Insect Behav (2010) 23:165–179 DOI 10.1007/s10905-010-9201-4 The Foraging Behavior of Lysiphlebus fabarum (Marshall), a Thelytokous Parasitoid of the Black Bean Aphid in Iran Arash Rasekh & J. P. Michaud & Hossein Allahyari & Qodratollah Sabahi Revised: 19 November 2009 /Accepted: 14 January 2010 / Published online: 8 February 2010 # Springer Science+Business Media, LLC 2010 Abstract A series of laboratory experiments examined the foraging behavior of a thelytokous strain of Lysiphlebus fabarum (Marshall), a strongly proovigenic parasitoid of Aphis fabae Scopoli, in Iran. Females use chemical camoflage to forage undisturbed in ant-tended aphid colonies and solicit honeydew from aphids in the manner of ants. Rates of oviposition are very low (∼ 1.2 eggs / h) despite many aphid encounters and persistent ovipositor probing which appears to prime aphids for subsequent honeydew solicitation. Starved females spent 3.6 times longer in host patches (leaf disks with 15 2nd–3rd instar A. fabae) than did females sated on honey, and 40% of this time was spent soliciting honeydew. Five d-old females spent longer in patches than did one d-old females, and parasitized three times as many aphids. A 24 h pre-trial foraging experience did not reduce mean egg load significantly compared to a one h experience, but was sufficient to reduce patch residence time and number of aphids parasitized. Wasps reared under short day conditions (L:D=10:14) were more pessimistic foragers (remained longer in patches and parasitized more aphids) than females raised under long days (L:D=16:8). Wasps that encountered aphids previously parasitized by conspecifics began to superparasitize and remained longer in patches than females that encountered only unparasitized aphids. Encounters with other females had no effect on foraging behavior, possibly because cuticular camoflage interferes with conspecific recognition. The exceptionally low oviposition rate of this wasp may reflect a life history in which individual fitness has evolved to be strongly dependent on continued ant attendance throughout the period of progeny development. A. Rasekh Department of Plant Protection, Shahid Chamran University of Ahvaz, Ahvaz, Iran J. P. Michaud (*) Kansas State University, Agricultural Research Center—Hays, 1232 240th Ave, Hays, KS 67601, USA e-mail: [email protected] H. Allahyari : Q. Sabahi Department of Plant Protection, College of Agriculture, University of Tehran, Karaj, Iran 166 J Insect Behav (2010) 23:165–179 Keywords Aphis fabae . ants . day length . honeydew . oviposition . patch residence time Introduction Foraging parasitoids often face uncertainty with respect to food and host availability and adjust their behavior according to the conditions they encounter. For example, a female’s propensity to search for hosts, or accept them after they are encountered, can be influenced by intrinsic factors such as age, egg load, nutritional status, mating status, etc. These have been referred to as ‘physiological state variables’ (Collins and Dixon 1986;Roitbergetal.1993; Sirot et al. 1997). Parasitoids may also learn from experience (Godfray and Waage 1988; Vet et al. 1990; Chow and Mackauer 1992) and environmental cues can guide adaptive responses to hosts and host patches, provided these are reliable indicators of current or future foraging conditions (e.g., host availability, relative host quality, intensity of competition, etc.). Furthermore, external cues may interact with internal states to modulate pivotal decisions in foraging behavior such as host acceptance and patch leaving (Lucchetta et al. 2007). Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) is a ubiquitous parasitoid of the black bean aphid, Aphis fabae Scopoli, in many agroecosystems (Starý 1986; Nuessly et al. 2004). This wasp has mainly thelytokous reproduction in central Europe (Nemec and Starý 1985; Starý 1986; Kavallieratos et al. 2008) where it has been recorded from 44 different aphid hosts (Kavallieratos et al. 2004; Tomanović et al. 2009) and frequently parasitizes A. fabae on both crops and weeds (Hildebrand et al. 1997; Völkl and Stechmann 1998). Many species of the genus Lysiphlebus are remarkable for cuticular lipids that closely mimic those of their aphid hosts (Liepert and Dettner 1993). These myrmecophilous species are able to forage with impunity in ant-tended aphid colonies and so garner the protection of ants for their progeny while they are in vulnerable immature stages within their hosts (Völkl 2000). We observed that our particular strain of L. fabarum also engaged in apparent ant mimicry behavior—the use of antennation to solicit honeydew directly from aphids (Rasekh et al. 2010). Despite a median longevity of only 4.5 d, this wasp is able to utilize a combination of chemical and behavioral mimicry to obtain resources and services from members of trophic levels both above and below it. Host-feeding on hemolymph is more common in synovigenic parasitoids that require a source of protein to mature their eggs (Godfray 1994). However, L. fabarum is largely proovigenic, emerging with several hundred mature eggs in its ovaries (Belshaw and Quicke 2003). Since honeydew is primarily a source of sugar, honeydew solicitation by L. fabarum likely substitutes for nectar-feeding in providing the energy that fuels foraging behavior, even though recent studies suggest that honeydew may be a generally inferior sugar source (Wackers et al. 2008; Wyckhuys et al. 2008). Patch residence time (PRT) is often a focal point of behavioral analysis for parasitoid species that exploit hosts with clumped distributions (Waage 1979; J Insect Behav (2010) 23:165–179 167 McNamara and Houston 1985; Godfray 1994). Charnov’s(1976) marginal value theorem can be extended from foraging for prey to foraging for patches; a rate- maximizing forager should select a patch residence time so that the marginal rate of fitness gain at the time of leaving equals the long term average rate of fitness gain in the habitat. However, parasitoids typically have little information about overall habitat quality, and this may be limited to a few recent experiences. Some behaviors typically occur outside the host patch (e.g., habitat-seeking, mate-seeking, or food- seeking) whereas others occur only within it (e.g., host attack, oviposition, decision to leave). However, thelytokous parasitoids avoid the time expenditure associated with seeking a mate (Price 1980), and also the cost of producing sons (Maynard Smith 1978). Parasitoids such as L. fabarum that feed directly from their hosts save even more time and energy by avoiding the need to search for food outside host patches (Jervis and Kidd 1986). Here it becomes more difficult to assign a discrete function to behaviors associated with host encounters, i.e., are they directed at acquiring food or parasitizing hosts? We made direct observations of L. fabarum within artificially constructed patches of its host, the black bean aphid, to explore its time allocation to behaviors associated with feeding and parasitism, while manipulating intrinsic and extrinsic factors that are predicted to impact these behaviors. Specifically, we hypothesized that females in a low-energy state (created by a period of starvation) would increase the proportion of time they allocated to soliciting honeydew at the expense of parasitism rate. We hypothesized that younger females would leave patches earlier and parasitize fewer aphids than older ones, and that long versus short pre-trial foraging experiences would produce the same effect. In addition, we hypothesized that females exposed to short day lengths, aphids previously parasitized by other females, or conspecific females, would remain longer in patches and parasitize more aphids relative to females receiving control experiences, since these signals are indicative of unfavorable reproductive conditions. Materials and Methods Insect Colonies A thelytokous colony of L. fabarum was established from mummies collected from black bean aphids infesting broad bean in a field in Zanjan Province, Iran, in June 2007. A stock colony of A. fabae was maintained on potted broad bean, V. faba var. Sarakhsi, grown in pots filled with fertilized sawdust in growth chambers at 20±1°C, 65–75% RH, and a 16:8 (L:D) photoperiod. The parasitoid was reared on A. fabae fed on broad bean under the same conditions. All aphids used in experiments were 4 d (± 6 h) old at 20°C (late 2nd–early 3rd instar nymphs). Synchronous cohorts of wasps were produced by exposing 2nd instar A. fabae to 3 d-old female wasps in a 5:1 ratio in ventilated plastic cylinders (8.0 cm diameter x 20.0 cm) for a period of 6 h and then transferring the aphids to potted bean plants in a growth chamber until mummies formed. Mummies were carefully removed from plants by scraping them gently off the leaves and then isolated in gelatin capsules 168 J Insect Behav (2010) 23:165–179 (vol.=0.95 cm3) until emergence, whereupon each adult female was released into her own ventilated plastic cylinder (3.5 cm diameter×7.0 cm) and provisioned with diluted honey (as droplets on a strip of wax paper) and water (on a cotton roll). The water was refreshed daily and the diluted honey every second day. Unless otherwise noted, all females had continuous access to food prior to testing andwereusedinexperimentswhentheywere72±4hofagewithoutprior exposure to aphids. All experiments were carried out on a laboratory bench under fluorescent light and an ambient temperature of 20°C within a climate-controlled, walk-in growth
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