Effect of host odor cues on behavioral responses of the spider wasp, Pepsis formosa (Hymenoptera: Pompilidae).
The ability of many species of animals to detect and respond to olfactory cues associated with predators and prey has been well documented (see reviews by Chapman et al. 1987; Kats & Dill 1998). Regarding the detection of potential prey by arthropod predators or parasitoids (Vinson 1985), a number of different proximal cues are known to affect patch choice, residence time, and assessment of suitability of prey, including visual and tactile cues as well as chemosensory cues associated with prey odors (olfaction).
The types of sensory cues used by arthropod herbivores and carnivores in the detection of plants or prey are diverse and vary according to microhabitat conditions and foraging strategies. Many orthopteran insects and lepidopteran larvae exhibit genetic or cognitive-based responses to specific chemical cues associated with food plants and utilize these cues to make decisions concerning the amount of time to spend in a particular patch before switching to another location (Bernays 1993). With respect to predators, the ability to utilize olfactory cues to detect prey has been demonstrated in many species, including crustaceans (Lima & Dill 1990; Chivers & Smith 1998), spiders (Foelix 1996), and insects (Bernays 1993; Punzo 1996). For example, the lynx spider Oxyopes salticus and wolf spider Trochosa parthenus, are capable of detecting odors associated with insect prey species, and will choose substrates associated with the odor of these insects over those that do not (Punzo 2002; Punzo & Kukoyi 1997).
Among parasitoid Hymenoptera, it is well known that many species rely on olfactory cues to identify their hosts after they have been located (Vinson 1985; Vet et al. 1991). In some species, the ability to detect and respond to host-specific odors is associated with a genetically-based (innate), hard-wired behavioral program (Doutt 1959), while host-finding behavior in other species may be affected by experience (learning) at various stages of the life cycle (see review by Turlings et al. 1993).
Spider wasps of the genus Pepsis (Hymenoptera: Pompilidae) are common inhabitants of North American deserts (Hurd 1952; Punzo 1994a; 2005). Nectivorous females selectively hunt theraphosid (tarantula) spiders as a food source (host) for their carnivorous larvae (Williams 1956; Punzo 1991). A spider is paralyzed and then dragged backwards over the ground and placed in a nest (Petrunkevitch 1926: 1952). A wasp may use the spider's burrow as its nest, or excavate one of its own (Evans & Eberhard 1970; Punzo 1994b). After depositing a single egg on the abdomen of the spider, the entrance to the nest is sealed and the wasp begins searching for another host (Passmore 1936; Cazier & Mortenson 1964). Although experimental evidence is lacking, it has been suggested that these wasps utilize species-specific olfactory cues to assess the suitability of a host spider (Lucas 1919; Petrunkevitch 1926; Punzo & Garman 1989). It is unclear whether or not pepsine wasps will utilize more than one species of theraphosid spider as a host in areas where two or more theraphosid species occur sympatrically (Punzo 2000; 2005).
Pepsis formosa (Say) has a wide geographical distribution and is found throughout most of Texas, westward into New Mexico, Arizona, Nevada and California (Hurd 1952). Previous studies on the biology of P. formosa include descriptions of various aspects of its natural history and ecology (Williams 1956; Cazier & Mortenson 1964; Punzo & Garman 1989; Punzo 2000) as well as a detailed description of hunting behavior exhibited by female wasps from the Big Bend region (Brewster County) of far west Texas (Punzo 1991).
In southern Texas (Hidalgo County), two species of tarantula spiders are found where P. formosa occurs: Aphonopelma harlungenum (Chamberlin) and A. heterops Chamberlin. The purpose of this study was to determine if P. formosa can detect and respond to olfactory cues associated with these tarantula spiders, and if one theraphosid species is preferred over the other.
MATERIALS AND METHODS
Subjects. -- All wasps were adult females of P. formosa and were collected with sweep nets within a 4-km radius of Elsa, Texas (Hidalgo County, USA) during August, 2003. All species of pepsine wasps collected were identified to species. Because it has been suggested that non-inseminated pepsine females will not hunt (Williams 1956; Punzo 2000), only those females of P. formosa who had been observed to mate with males were used in subsequent experiments (n = 90). Females were collected immediately after they were observed mating in the field.
Wasps were transported back to the laboratory and placed individually in cylindrical glass containers (40 cm in length, 7 cm in diameter) where they were provided with water ad libitum and fed on a diet consisting of honey mixed with a glucose solution. Wasps were maintained at 22 [+ or -] 0.2[degrees]C, 62-65% relative humidity, and 12L:12D photoperiod regime in Percival Model 85A environmental chambers (Boone, Iowa, USA).
Examination of hosts and burrows. -- All tarantulas found wandering over the surface of the ground were collected and identified to species, and their body weights and sex recorded. Whenever a tarantula burrow was located, it was excavated to determine if a spider was present, the species of spider, and whether it had been paralyzed and had an egg or larva attached to its abdomen. The sex of spiders was also recorded. All parasitized spiders (n = 134) were transported back to the laboratory and maintained under constant darkness at 22 [+ or -] 0.2[degrees]C and 62-65% RH in environmental chambers. Attached eggs and larvae were allowed to complete development, and after eclosion, parasitoids were identified to genus and species.
Experimental design and behavioral testing. -- Chemical stimuli (treatments) were obtained from theraphosid spiders (A. harlingenum and A. heterops) (Araneae: Theraphosidae) as well as from the mealworm beetle, Tenebrio molitor (Coleoptera: Tenebrionidae). Tenebrio molitor is a pest of stored grains and is not likely to be encountered by these wasps. Both species of spiders were collected from the same areas inhabited by P. formosa. Pieces of absorbent filter paper (Whatman No. 612, Carolina Biological Supply Co., Burlington, North Carolina, USA) were conditioned with odors associated with these arthropods by placing paper on the floors of cages that housed spiders and beetles for a period of one week prior to testing.
The response of individual wasps exposed to these three different chemical stimuli was tested. For each trial, half of the floor of a rectangular plastic chamber (30 by 15 by 8 cm) was lined with a piece of paper that was moistened with dechlorinated tap water (control side). The other half (treatment side) was lined with paper that had been conditioned with chemosensory cues associated with A. Harlingenum, A. heterops, or T. molitor. The two pieces of paper were separated by a distance of 2 cm to minimize contamination of chemical stimuli between the two sides. After the pieces of paper were placed on each side of the chamber, they were sprayed with dechlorinated tap water to saturate the papers. This ensured that any differences in the response of wasps to treatment versus control papers could be attributed to chemical cues and not to moisture level. Walls of the chamber were sprayed with Fluon[R] (Central Scientific, Chicago, Illinois) to prevent wasps from climbing up on them. Observations were made through a one-way mirror to minimize disturbances to test subjects.
At the start of each trial, an individual female wasp was grasped gently with forceps and placed into the center of the chamber. At 30-min intervals, over a 3-hr period, the location of the test subject on the control or treatment paper was recorded. If a wasp was located at the center of the floor, the position of the head and antennae was used to assign location. The chamber was rotated 1800 every 30 min during testing to control for the possibility of any bias in the wasp's orientation in the chamber.
Thirty different wasps in each of the three treatments (90 tests) were tested. Individual wasps were used in only one test. For each trial, the number of times each wasp was located on the treatment side of the chamber out of a possible five observations (one per 30 min for 150 min = five observations) was summed. For each of the three treatments a comparison of whether wasps spent significantly more time than expected on a particular side of the chamber was compared using a Wilcoxon Signed Rank test (Sokal & Rohlf 1995). A similar behavioral bioassay for testing responses of animals to chemical stimuli has been used in studies on a variety of taxa including vertebrates (Chivers & Smith 1998) and other species of invertebrates (Kats & Dill 1998).
The total number of males and females (spiders within burrows plus spiders wandering at the surface of the ground) of A. harlingenum was 252 and 185, respectively, as compared to 238 and 172, for A. heterops, indicating that these two theraphosids occur at similar densities at this study site. The number of burrows containing A. harlingenum (112) and A. heterops (103) was also similar. There was no significant difference between the mean body weights for males and females of A. harlingenum (Ms: 6.8g [+ or -] 0.8 SE; Fs: 9.8 [+ or -] 1.2g) and A. heterops (6.6 [+ or -] 0.4; 9.7 [+ or -] 0.5) (t test, P > 0.50).
With respect to wasps, P. formosa was more common than other pepsine wasps. From a total of 786 adult wasps collected during the course of this study, 532 (67.7%; 284 males, 248 females) consisted of P. formosa, 88 (11.1%; 48, 40) were P. thisbe, and 166 (21.2%; 89, 77) were P. cerberus.
All species of pepsine wasps associated with paralyzed host spiders found in the field are listed in Table 1. Out of 112 parasitized A. harlingenum found, 82 (73.2%) were females, as compared to 78 of 103 (75.7%) for A. heterops (Chi Square contingency test: [X.sup.2] = 57.43, P < 0.001, and 45.09, P < 0.001, respectively).
All wasps found at this time of the year were in various larval stages. Of the 103 P. formosa larvae, 90.3% were associated with A. harlingenum as compared to only 9.7% for A. heterops (Table 1). The other two species of pepsine wasps also utilized A. harlingenum and A. heterops as hosts.
The responses of the 90 female wasps to papers containing various treatment odors are shown in Fig. 1. Wasps spent signifycantly more time on paper conditioned with the odors associated with A. harlingenum, as compared to paper containing olfactory stimuli from A. heterops (Z = 3.92, P < 0.001) or the beetle, T. molitor (Z = 3.88, P < 0.001). In fact, there was no significant difference in the way P. formosa responded to odors of A. heterops or the novel stimuli associated with the beetle, T. molitor (P > 0.60).
When wasps were introduced into the test chamber they waved their antennae in the air, and also used them to tap the floor as they moved quickly over the floor of the chamber. When making contact with paper conditioned with odors from A. harlingenum, wasps typically exhibited a series of circular movements localized to a particular region of that paper, and their general level of activity increased. Eighty-one of the 90 wasps (90%) were also observed to periodically extrude their stinger, making contact with the floor of the chamber. In contrast, this behavior was exhibited by only 6 wasps (6.7%) when walking on paper conditioned with odors from A. heterops or T. molitor.
[FIGURE 1 OMITTED]
Results showed that P. formosa was the most common pepsine wasp at this location and that females chose A. harlingenum as a host far more frequently than A. heterops. Because these spiders were of similar size and present in similar numbers, this difference in host choice must be the result of specific cues associated with these spiders that are used by P. formosa in making decisions on host selection, perhaps including olfactory cues, rather than host size or availability. In addition, because the wasps used in these experiments were collected as adults, and the species of host upon which they completed their larval development unknown, no conclusions can be reached concerning the possible role that larval olfactory imprinting may have played in their subsequent choice of hosts as adults.
The majority of spiders paralyzed by P. formosa were females. Because of their larger body size, female spiders provide more food for developing wasp larvae. Larvae provided with larger hosts attain a larger adult body size (Lucas 1919; Field 1992). It is known that larger body size in pepsine wasps is correlated with a higher number of eggs produced per female (Evans & Eberhard 1970; Punzo 2000; 2005). However, it is not known whether female wasps reject male spiders in favor of females, choose males as hosts only when female spiders cannot be located, or are opportunistic hunters and select spiders as they are encountered in the field.
In contrast, other species of pepsine wasps that occur sympatrically with P. formosa at this location (P. thisbe and P. cerberus) selected A. heterops as a host more frequently than A. harlingenum. This type of resource partitioning may reduce competition between this guild of parasitoid wasps that all utilize theraphosid spiders as hosts. Further studies should be conducted to test this hypothesis.
Predators may use a variety of prey-associated cues to locate potential prey, including visual, mechanical, and chemical stimuli (Chapman et al. 1987). Results from this experiment show that wasps were able to detect olfactory cues associated with A. harlingenum and spent more time on substrates conditioned with odors associated with this spider than on those containing cues from A. heterops or T. molitor. This is in agreement with studies on other species of invertebrate predators responding to olfactory cues associated with their prey, including muricid snails (Carriker & Zandt 1972), tiger beetles (Wilson 1978), ants, (Holldobler & Wilson 1994), and other species of solitary wasps (Evans & Eberhard 1970; Turlings et al. 1993). In the case of arachnids, field-collected lynx and wolf spiders showed a significant preference for substrates containing olfactory cues associated with field crickets, a common prey species (Punzo & Kukoyi 1997).
The ability to detect and respond to stimuli associated with suitable prey will reduce energy and time expended in random search. This should improve hunting success while minimizing the probability of encountering other predators known to capture and ingest pepsine wasps such as roadrunners, grasshopper mice, wolf spiders, solifugids, and mantids (Punzo 1998; 2000), all of which are found at this study site. Further studies should be conducted on captive-bred wasps that have had no previous experience with theraphosid spiders to determine whether their ability to respond to host olfactory cues is primarily innate or dependent to some degree on adult learning or larval olfactory imprinting.
I thank R. J. Edwards, L. Ludwig, S. B. Vinson, and anonymous reviewers for comments on an earlier version of the manuscript, A. Jenzarli for consultation on statistical procedures, and C. Farmer for assistance in maintaining animals in the laboratory.
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Table 1. Species of pepsine wasp larvae associated with tarantula (Theraphosidae) spider hosts in Hidalgo County, Texas. Data represent the number of each species of pepsine wasp found in a total of 215 spider burrows. Two species of theraphosids were found at this study site: Aphonoplema harlingenum and A. heterops. Paralyzed spiders were excavated from their burrows and the attached wasps eggs or larva allowed to complete development in the laboratory for subsequent identification of emergent adult wasps. Spider burrows Pepsine wasp Aphonopelma harlingenum Aphonopelma heterops Pepsis formosa 93 10 Pepsis thisbe 11 61 Pepsis cerberus 8 32 Total 112 103
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|Publication:||The Texas Journal of Science|
|Date:||Feb 1, 2006|
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