Odor-Based Recognition of Nectar in Cursorial Spiders
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DOI: 10.1111/j.1570-7458.2008.00669.x Blackwell Publishing Ltd Odor-based recognition of nectar in cursorial spiders Joseph M. Patt* & Robert S. Pfannenstiel USDA–Agricultural Research Service, Subtropical Agricultural Research Center, Weslaco, TX 78596, USA Accepted: 18 December 2007 Key words: foraging, nectarivory, learning, olfaction, chemosensory, signals, local search, plant defense, biological control, Hibana futilis, Araneae, Anyphaenidae Abstract Carnivorous arthropods are known to rely on non-prey foods, such as honeydew, pollen, and nectar. Consumption of plant-based nutrients by spiders also appears to be widespread, especially in cursorial species. This is not surprising, as studies have shown that these spiders’ activity levels, survivorship, and reproduction are increased when their diet includes plant-based nutrients, especially under conditions of prey scarcity. However, the sensory and behavioral means by which they recognize and locate non-prey food is unknown. Here we show that immatures of a nectarivorous spider [Hibana futilis Banks (Araneae: Anyphaenidae)] can recognize and remember particular chemical stimuli associated with nectar. Following ingestion of minute amounts of sugar, these spiders exhibited counterturning and other local searching behaviors that increased their chances of finding more nectar. When placed on test arenas, spiders that were naïve with respect to nectar aroma located artificial nectaries composed of diluted honey significantly faster than unscented nectaries composed of 1 sucrose solution. These results indicate that H. futilis is neurophysiologically and behaviorally adapted for recognizing olfactory stimuli. Interestingly, only spiders that ingested sugar and were engaged in local search responded to nectar aroma, suggesting that stimulation into local search is necessary to prime olfactory responses. We found that H. futilis could be conditioned to associate the presence of nectar with a novel aroma, in this case vanilla, and remember this aroma over the course of several hours. In arenas with vanilla-scented nectaries, spiders that had previous experience feeding on vanilla- scented sucrose droplets located the nectaries significantly faster than did vanilla-naïve spiders. The capacity to remember specific aromas could enhance the spiders’ ability to find nectar, either when moving between different parts of the same plant or among different plant species. The results here indicate that nectarivorous spiders possess the sensory capabilities and programed behaviors necessary for efficient detection, recognition, and location of nectar sources. ghost spiders (Anyphaenidae), and sac spiders (Miturgidae Introduction and Clubionidae). Rather than relying on webs, these There is an increasing awareness of the central role that spiders actively search or lie in ambush for their prey non-prey foods, such as honeydew, pollen, and nectar, play (Pollard et al., 1995; Jackson et al., 2001). Cursorial in the lives of carnivorous arthropods (Wäckers et al., spiders, in general, use a variety of chemical stimuli to 2005). Their activity levels, development, survivorship, detect and recognize different resources, including mating success, and fecundity can be enhanced by prey, predators, mates, and hunting sites (Jackson & Pollard, consumption of non-prey food, especially during periods 1996; Persons & Rypstra, 2000; Jackson et al., 2002a,b,c, of prey scarcity (Smith & Mommsen, 1984; Vogelei & 2005; Heiling et al., 2004; Roberts et al., 2007). The cognitive Greissl, 1989; Pollard et al., 1995; Taylor & Foster, 1996; abilities of these spiders are considerable, extending to the Wäckers et al., 2005). Nectarivory is now known to be a ability to make decisions about prey-specific stalking common occurrence in at least five families of spiders routes (Jackson et al., 2001), selective attention to potential (Taylor & Foster, 1996; Jackson et al., 2001), including the prey occupied with their own foraging tasks (Jackson et al., jumping spiders (Salticidae), crab spiders (Thomisidae), 2002a,b,c), and multimodal (VanderSal & Hebets, 2007) and contextual learning (Skow & Jakob, 2006). This *Correspondence: E-mail: [email protected] suggested to us that they use chemical cues to detect and © 2008 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 127:64–71, 2008 No claim to original US government works 64 Journal compilation © 2008 The Netherlands Entomological Society Recognition of nectar odor by spiders 65 locate nectaries and may learn to recognize specific cues associated with nectar. The purpose of this study was to determine whether nectarivorous spiders respond to gustatory and olfactory stimuli associated with nectar, and use these cues to detect and locate nectaries. We also wanted to determine if they could learn to recognize olfactory stimuli associated with nectar. The subjects of our study – immatures of a ghost spider, Hibana futilis Banks (Araneae: Anyphaenidae), forage for eggs and small prey while running across foliage (Pfannenstiel, 2005) – a searching strategy that may frequently bring them into proximity with flowers or extra-floral nectar glands. The addition of sucrose to their diet increases their survivorship and enables them to complete development when provided with only minimal prey (Taylor, 2004, Taylor & Pfannenstiel, unpubl.). Using the cold anthrone test, Taylor (2004) showed that 32% of female and 10% of male H. futilis were positive for nectar Figure 1 sugars in cotton fields. Given the benefits they receive from Diagram of the Hibana futilis test arena showing arrangement of artificial nectaries in the perimeter zone nectar consumption, we anticipated that immature H. futilis (perimeter nectaries; PN) and center zone (center nectaries; CN) possessed sensory and behavioral adaptations to enable (not to scale). Different combinations of scented and unscented them to efficiently detect and locate nectaries. artificial nectars were used to test for stimulation into local search and response to nectar aroma. Spiders were released in the Materials and methods perimeter zone halfway between two PN. We measured the behavioral responses of immature H. futilis to nectar stimuli on test arenas constructed from glass Petri dishes (Figure 1) in the laboratory. In the TX, USA. Spiders were reared individually in Petri dishes experiments described below, simulated ‘nectaries’ composed and kept in an incubator under an L15:D9 regime at of small droplets of artificial nectar were positioned in the 26 ± 1 °C. They were fed with moth [Helicoverpa zea arena center and perimeter (Figure 1). During pre-tests, (Boddie)] eggs ad libitum until they molted twice. Water spiders placed on an ordinary Petri dish displayed typical was provided continuously with a moistened cotton wick. thigmotaxis, that is, they showed a strong tendency to To improve their responsiveness during the experiments, crawl along the arena perimeter, and only occasionally spiders were starved prior to testing (J Patt, unpubl.). moved across the face of the dish. Therefore, on arenas When individuals began their molt to third instar, all with nectaries, departure from the perimeter to the remaining moth eggs were removed from their culture arena center was indicative of a response to nectar stimuli. dishes and then withheld following their emergence. To We conjectured that contact with the perimeter nectaries ensure that they were aroma-naïve, spiders were kept in the (PN) would stimulate local search, a behavioral state incubator and were never exposed to any of the stimuli (Dethier, 1976; Bell, 1991) in which animals frequently used in the experiments. Because H. futilis is nocturnal counterturn and reverse direction to increase their (Pfannenstiel, 2005), they were maintained on a reverse probability of locating a resource. Likewise, if the spiders photocycle to permit daytime testing. were stimulated by nectar aroma, then their movements Only spiders that were actively moving within their would direct them toward the arena center, the area with culture dishes when inspected at testing time were used in the highest aroma concentration. These behaviors, the experiments. Individuals that were hidden in their especially when expressed simultaneously, would enhance silken retreat tubes or otherwise quiescent in their culture their ability to recognize and locate the nectaries located in dishes were not selected. Because the spiders became very the arena center. agitated when handled, each individual was anesthetized by gentle chilling for 60 s just prior to testing. Chilling was Spiders accomplished by transferring a culture dish with its spider All tests used third instars of the ghost spider, H. futilis, from the incubator into a –12 °C freezer. Once anesthetized, that were F1 progeny of wild females collected in Weslaco, the spider was immediately transferred from its culture dish 66 Patt & Pfannenstiel Table 1 Treatments and behaviors examined during experiments testing stimulation into local search, responses to nectar aroma, and effect of local search on responses to nectar aroma by Hibana futilis Perimeter ‘nectaries’ Center ‘nectaries’ (CN) Behavior tested Treatment (PN) blank or present unscented or scented Stimulation into searching behavior Control Blank Unscented following sugar ingestion Experimental Present Unscented Responses to nectar aroma Control Present Unscented during local search Experimental Present Honey-scented Responses to nectar aroma Control Absent Unscented without