Host-seeking behavior in larvae of the robber fly Mallophora ruficauda (Diptera: Asilidae)
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1 Journal of Insect Physiology 50 (2004) Host-seeking behavior in larvae of the robber fly Mallophora ruficauda (Diptera: Asilidae) Marcela K. Castelo a,, Claudio R. Lazzari a,b a Laboratorio de Fisiología de Insectos, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4to piso, (C1428EHA) Buenos Aires, Argentina b Institut de Recherche sur la Biologie de l Insecte, UMR CNRS 6035, Université François Rabelais, Tours, France Received 29 July 2003; received in revised form2 February 2004; accepted 3 February 2004 Abstract The robber fly Mallophora ruficauda is the most important pest of apiculture in the Pampas region of Argentina. Adults prey on honeybees and other insects, while larvae parasitize larvae of scarab beetles, which live underground. Females of M. ruficauda do not search for hosts but instead lay eggs in tall pastures. Once hatched, larvae drop to the ground and burrow underground to search for their hosts. We tested in the laboratory whether larvae of M. ruficauda actively search for their hosts using host and/or host-related chemical cues. We report that M. ruficauda detects its host using chemical cues that originate in the posterior half of the host s body, most likely from an abdominal exocrine structure. This particular host-searching strategy is described for the first time in Asilidae. # 2004 Elsevier Ltd. All rights reserved. Keywords: Asilidae; Parasitoids; Host location; Scarabaeidae; Semiochemicals 1. Introduction Females of most parasitoids actively locate their hosts and lay eggs on their bodies. They normally find their hosts by using chemical cues (semiochemicals) released by the host (Lewis and Martin, 1990; Steinberg et al., 1993; Tumlinson et al., 1993; Udayagiri and Jones, 1992; Vet and Groenewold, 1990; Vet et al., 1990; Vinson, 1984). Semiochemicals convey information about the host and act as kairomones for the parasitoid, allowing location, recognition and selection of hosts (Lewis and Martin, 1990; Noldus, 1989; Papaj and Vet, 1990; Steinberg et al., 1993; Tumlinson et al., 1993; Turlings et al., 1991, 1993; Van Alphen and Vet, 1986; Vet and Groenewold, 1990; Vet et al., 1990; Vinson, 1984; Whitman and Eller, 1992). Females of most dipteran parasitoids, in contrast to many hymenopteran parasitoids, do not actively search for hosts. They lack a well-developed ovipositor and Corresponding author. Tel.: ; fax: address: mcastelo@uolsinectis.com.ar (M.K. Castelo). thus cannot insert their eggs into the body of the host (Feener and Brown, 1997; Godfray, 1994). Instead, they lay eggs at sites associated with the presence of the host. As a consequence, once hatched, larvae must locate their hosts by themselves (Clausen, 1940; Hagen, 1964; Roth et al., 1978). This type of active host location has been reported for larvae of Diptera and Coleoptera (Godfray, 1994). Even though information about host detection is scarce, it is generally believed that precise active mechanisms mediate the behavior (Eggleton and Belshaw, 1992; Feener and Brown, 1997). Furthermore, some parasitic larvae exhibit specific developmental and morphological adaptations for mobility. Among them, two general kinds of highly mobile larvae have been reported, i.e., triungulin and planidium. Concerning Asilidae, Musso (1978, 1981) has described the morphology of first-instar larvae as a typical planidium. However, whether or not that is related to the host-seeking behavior of Asilidae has not been established. Larvae of Mallophora ruficauda Wiedemann are mobile since birth. After hatching from egg-clusters laid by females on tall vegetation, larvae are dispersed /$ - see front matter # 2004 Elsevier Ltd. All rights reserved. doi: /j.jinsphys
2 332 M.K. Castelo, C.R. Lazzari / Journal of Insect Physiology 50 (2004) by the wind and fall to the ground (Castelo, 2003). Once on the soil, parasitoid larvae immediately begin to performdigging movements with their whole body in order to bury themselves and thus find their hosts. Fromthen on, survival of the larvae depends on a precise spatio-temporal matching between the distributions of hosts and parasitoids. But the high selectivity of M. ruficauda for it host, Cyclocephala signaticollis Burmeister (Coleoptera: Scarabaeidae), detected in places where several species of white grubs coexist (Castelo and Capurro, 2000), suggests that these parasitoid larvae actively search for and detect their hosts. The aims of this work are: (1) to test experimentally whether M. ruficauda larvae are able to actively search for and find their hosts, (2) to analyze whether host parasitoid encounters are mediated by host and/or host-related chemical cues, and (3) to find the location of such chemical cues within the body of the host. 2. Materials and methods First- and second-instar larvae of the parasitoid M. ruficauda were used throughout. Larvae were reared in the laboratory fromegg-clusters collected from grasslands associated with apiaries in Mercedes (34 v 40 0 S, 59 v 26 0 W, Buenos Aires province, Argentine). Once in the laboratory, they were maintained at room temperature and under natural illumination. Third-instar larvae of white grubs C. signaticollis (the host) were obtained directly fromsoil samples collected at the same place, and maintained in the laboratory in individual cages with soil at roomtemperature and in darkness. Hosts were fed weekly with pieces of potato. Trials were performed using rectangular experimental arenas (4:0 7:5 cm) divided into three equalsize zones (a middle one and two laterals) along the long axis. At each lateral zone, either a stimulus source or the corresponding control was presented. In the middle zone of the arena a single larva was released at a time. After 1.5 h, we recorded the location of the larva in the arena (i.e., the selection of a given lateral zone) Response of M. ruficauda to a live host in its breeding ground In this experiment, we presented in one lateral side of the arena one live host together with its breeding substrate (i.e., the soil, grub feces and other products of grub activity, such as material for refuge building). The other lateral side of the arena (control) contained clean soil fromthe same area. In this and all the experiments described below, the position of the stimulus was randomly changed between trials Response to the host environment The components of the stimuli used in the previous experiment were assayed separately in order to study which acted as orientation cues for the parasitoid larvae. Four experimental groups were studied Live hosts only One host (without substrate), confined by means of a plastic mesh to one lateral zone of the arena, was offered in one lateral side of the arena. The other lateral zone remained empty Host breeding substrate One lateral zone offered substrate that had been previously in contact with white grubs (grubs were removed). The other lateral zone contained clean substrate (i.e., without any previous contact with grubs) Host fresh feces Fresh feces froma single host, collected in pieces of filter paper (2:0 1:0 cm), were offered in one lateral zone. The other lateral zone contained a piece of clean filter paper Feces extracts Feces from10 white grubs were collected and diluted in 3 ml of hexane. A piece of filter paper (2:0 1:0 cm) containing 10 ll of that solution was presented in one lateral side. The other lateral side contained a piece of filter paper with 10 ll hexane Response to cuticular extracts from the host In this experiment, we tested the response of larvae of M. ruficauda to extracts of whole hosts prepared using different solvents. Ten white grubs were rinsed in 25 ml of solvent (either hexane, ethanol, or distilled water) for 15 min in order to extract substances associated with the cuticle and exocrine glands of the host. Thereafter, 10 ll of extract was placed on a piece of filter paper (2:0 1:0 cm) and tested against a piece of filter paper impregnated with 10 ll of the solvent alone Response to extracts of different portions of the host body In this experiment, we divided the host body in halves and homogenized each part using different solvents (half grub/ml of solvent). Pieces of filter paper (2:0 1:0 cm) were impregnated with 10 ll of the liquid fraction. The response of larvae of M. ruficauda to these extracts was tested against the response to papers impregnated with 10 ll of the corresponding solvent (control). The following homogenates were
3 assayed: (a) anterior body half in distilled water, (b) anterior body half in hexane, (c) posterior body half in distilled water, and (d) posterior body half in hexane Response to extracts of different host organs M.K. Castelo, C.R. Lazzari / Journal of Insect Physiology 50 (2004) This experiment was similar to the previous one, but we used different portions of the posterior half of the host homogenized in hexane. The goal of this experiment was to find which part of the posterior part of the host contained the attractive signal. We conducted five experimental series using: (a) the hindgut, (b) the posterior cuticle, (c) feces collected frominside the hindgut, (d) the hindgut wall (without feces), and (e) the raster (terminal cuticle of abdomen with setae). Experimental solutions were made using either a single white grub/ml of solvent (experimental series a d) or two grubs/ml of solvent (experimental series e, due to the small size of the raster). Pieces of filter paper (2:0 1:0 cm) were impregnated with 10 ll of extract and tested against a filter paper impregnated with 10 ll of hexane. Experiments were conducted under complete darkness, at 25 v C and 50% relative humidity. In all cases, stimuli and control sources were replaced after each trial. Ninety-six larvae were used per treatment. Each larva was used only once. In all experimental series, the preference of insects for either lateral side of the arena (control vs. experimental) was tested against a random distribution by means of v 2 tests of goodness of fit (i.e., 50% of choices for either side of the arena) (Rosner, 1995). Individuals that remained in the middle zone without making a decision were excluded from the analysis. 3. Results Our experiments showed that larvae of both first and of second instar exhibited similar responses when confronted with the task of locating a host Response to a live host and its breeding ground In this assay, larvae significantly chose the side of the arena presenting the live host with its breeding environment (v 2 ¼ 7:23; df ¼ 60; P < 0:05; Fig. 1) Response to host environment Larvae significantly chose the area occupied by a live host (v 2 ¼ 8:97; df ¼ 58; P < 0:05; Fig. 1). In the experimental series where different host-related cues were offered against a control, larvae distributed at random(series with feces only: v 2 ¼ 0:16, df ¼ 56; Fig. 1. Response of M. ruficauda larvae to their host C. signaticollis and its breeding substrate. Larvae of the parasitoid were collected near the live host. Abbreviations: Hþ S, host plus breeding substrate; H, host alone; F, feces; S þ F; substrate plus feces and other substances; F h, feces in hexane; asterisks denote statistically significant responses (v 2, P < 0:05). feces in hexane: v 2 ¼ 0:06, df ¼ 65; other series: substrate þ feces þ others, v 2 ¼ 2:68, df ¼ 63; Fig. 1) Response to cuticular extracts of the host In all cases, larvae distributed at randomin the experimental arena (distilled water extract: v 2 ¼ 1:80, df ¼ 44; ethanol extract: v 2 ¼ 0:23, df ¼ 38; hexane extract: v 2 ¼ 0:08, df ¼ 51) Response to extracts of different portions of the host body Larvae significantly preferred the side of the arena that offered the paper impregnated with the hexane extract of the posterior half of the host body (v 2 ¼ 8:14; df ¼ 64; P < 0:05). In the rest of the experimental series, larvae were distributed at random (aqueous extracts of the anterior half of the body: v 2 ¼ 0:00, df ¼ 61; extracts of the anterior half of the body in hexane: v 2 ¼ 0:38, df ¼ 64; aqueous extracts of the posterior half of the body: v 2 ¼ 1:86, df ¼ 64; Fig. 2) Response to extracts of different host organs Larvae significantly chose the side of the arena offering the paper impregnated with extracts of the host hindgut (v 2 ¼ 4:19; df ¼ 68; P < 0:05). Choices in the remainder of the experimental series were not different fromrandom(extracts of the posterior cuticle: v 2 ¼ 0:01, df ¼ 68; feces collected fromthe gut of the host: v 2 ¼ 1:25, df ¼ 65; gut wall: v 2 ¼ 1:92, df ¼ 51; raster: v 2 ¼ 0:24, df ¼ 65; Fig. 3).
4 334 M.K. Castelo, C.R. Lazzari / Journal of Insect Physiology 50 (2004) Fig. 2. Response of M. ruficauda larvae to extracts fromthe anterior or posterior parts of the host body. Larvae significantly oriented towards the hexane extract of the posterior half of the host body. Aqueous extracts and extracts made with the anterior half did not elicit significant responses. ABw, anterior body half in distilled water; PBw, posterior body half in distilled water; ABh, anterior body half in hexane; PBh, posterior body half in hexane; asterisk denote statistically significant responses (v 2, P < 0:05). Fig. 3. Response of M. ruficauda larvae to extracts obtained from different organs of the host body. Larvae oriented towards hexane extracts of the host hindgut. HG, hindgut; PC, posterior cuticle; FD, feces obtained by dissection; HGW, hindgut wall; R, raster; asterisk denote statistically significant responses (v 2, P < 0:05). 4. Discussion The development of a mobile larval stage (planidium) enables the exploitation of previously inaccessible, concealed host species by some parasitoids (Price, 1975). Parasitoid species with host-seeking larvae, other than M. ruficauda, possess different strategies to find their hosts. In general, females make that choice by laying eggs in appropriate places. For example, when a female of Homotrixa alleni (Diptera: Tachinidae), Ormia depleta (Diptera: Tachinidae), or Blaesoxipha flies (Diptera: Sarcophagidae) detects the proximity of concealed hosts, she powerfully releases larvae, which disperse over distances. This way, females increase the chances of the larvae to find a host and therefore to establish successful parasitism(allen and Pape, 1996; Allen et al., 1999). In most cases, however, larvae play a passive role, i.e., they do not respond to chemical, visual and/or vibratory cues fromthe host. Instead, they wait for the host to pass nearby, a strategy that is presumed to result in unspecific parasitism and high superparasitism(allen, 1995; Allen et al., 1999; Fowler and Martini, 1993; Walker and Wineriter, 1991). In other parasitoid species, mostly Diptera and Coleoptera, both the female and the larvae are involved in the finding of suitable hosts (Eggleton and Belshaw, 1992). For example, the female of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae) oviposits on the soil near plants infested by the host, and the larvae seek and discriminate hosts by means of chemical cues (Royer et al., 1999). In M. ruficauda, both the female and the larva play a role in the success of parasitism because both contribute to finding the host. Although females of this species do not exhibit classical hostseeking behavior, they contribute to host finding by selectively laying eggs in plants of adequate heights. This selectivity for ovipositing on high sites might favor the dispersal of larvae and thus might constitute a strategy that optimizes the probability of parasitism in the field (Castelo and Corley, in press). Furthermore, larvae of M. ruficauda selectively parasitize certain species of grub larvae (Castelo and Capurro, 2000). This selectivity was also observed in other families of Diptera parasitoids having planidiumlarvae, such as Acroceridae and Tachinidae (Allen, 1995; Allen et al., 1999; Roth et al., 1978). M. ruficauda exhibits some non-typical parasitoid behaviors. As already mentioned, females of this species do not oviposit directly on their hosts, but on vegetation. Our results suggest that M. ruficauda larvae might behave as a true planidium: in the field they are able to find their hosts after being dispersed by the wind, and they possess the typical setae found in ectoparasitic Diptera. In addition, the first and second instars do not differ in their morphology, except for a slight increase in size. In our experiments, both firstand second-instar larvae exhibited similar responses when confronted with the task of locating a host. This fact reveals that host-searching is not limited, in this species, to recently hatched larvae. We observed that, if no host was offered, second-instar larvae (but not firstinstar larvae) die before molting to the following instar. Thus, first-instar larvae can complete their development by using nutritional reserves or by finding food sources other than living hosts. Although it has been
5 M.K. Castelo, C.R. Lazzari / Journal of Insect Physiology 50 (2004) reported that some Asilidae exhibit different strategies for obtaining and using nutrients (Musso, 1983), in the case of M. ruficauda, our observations indicate that the use of reserves or the absorption of nutrients from the soil is limited to the first instar. Our results indicate that larvae of M. ruficauda exploit chemical cues associated with the posterior half of the body of their hosts. It is known that some coleopteran larvae possess secreting structures associated with the hindgut, some of them of unknown function. The mid- and the hindgut have epithelial cells with different appearances, depending on the larva s feeding habits (Areekul, 1957). Many of these cells and associated structures release their secretory products into the gut lumen, where they mix with the gut contents, and thus can be found in the feces. Rogers and Potter (2002) reported that white grub feces of two species of Cyclocephala and Popilia japonica Newman attract parasitoid wasps of the Thipia genus. Also, these authors observed that these wasps are able to discriminate among different species of white grubs, suggesting that the feces of each species contain specific kairomones. The evidence from our experiments indicates that this is not the case in the host parasitoid systemwe studied, because neither feces, nor the content of the hindgut, attracted the parasitoid. Concerning the orientation mechanism involved, our experiments probed the ability of larvae to orient to the host and/or host-related chemicals using gradients. Under natural conditions, M. ruficauda larvae search for hosts underground. Thus, the possibility that larvae orient towards their hosts by means of an anaemotactic mechanism (i.e., orientated response to a flow carrying the odorous molecule) has to be discarded. In that regard, it should be noted that the results of our experiments, where no airstreams were offered, indicate that both detection and orientation to the host are guided by true chemotactic behavior. This means that the larvae of M. ruficauda are able to detect and utilize concentration gradients established by volatiles from the host. Given that the host parasitoid encounter takes place in a medium (the soil) with particular chemical and adsorptive capacities, the signal has to have chemical characteristics that allow it to spread in soil, thus allowing the parasitoid to detect it. Our experiments indicate that the signal is non-polar, as extracts made with hexane, but not with water, are effective in orienting the parasitoid. On the other hand, the signal has to be relatively volatile to allow diffusion through the soil. The isolation of the source of the volatile/s will allow a better chemical characterization in the future. In summary, our results clearly demonstrate that M. ruficauda larvae are able to actively locate their hosts within the soil using chemical information. To our knowledge, this searching behavior has never been reported previously for Asilidae. Moreover, our results show that this response is mediated by chemical cues originated in the body of the host. We showed that these host-derived infochemicals are not associated with the cuticle or feces of the host. The source of the stimuli appears to be located in the posterior half of the body of the host. We presented here a simple and reproducible bioassay that can be used to study host-finding behavior mediated by chemical cues in soil parasitic insects. Our results show that larvae of the parasitoid M. ruficauda are attracted to volatiles produced by its hosts. The identification of the origin and chemical nature of the substance/s responsible for the attraction of M. ruficauda towards C. signaticollis will help us understand the particularities of this host parasitoid systemand might contribute to the development of novel strategies for controlling this pest. Acknowledgements We thank local beekeepers frommercedes province of Buenos Aires, Argentina, for allowing us to work on their farms. We also acknowledge J. Corley and C. Reisenman for critically reading and greatly improving the manuscript, and the staff of the Laboratory of Insect Physiology for valuable discussions. Thanks are also given to two anonymous reviewers for valuable comments. This work has been partially funded through grants PIP-CONICET No. 0529/98 (to A. Capurro), SeCyT-ECOS Programbetween France and Argentina No. A98B05 (to J. Corley and C. Bernstein) and fromthe University of Buenos Aires (to C. Lazzari). M. 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