International Journal of Comparative Psychology, 2006, 19 , 268-281. Copyright 2006 by the International Society for Comparative Psychology Spatial Learning in Dragonflies Perri K. Eason University of Louisville, U.S.A. Paul V. Switzer Eastern Illinois University, U.S.A. Spatial learning is evident in dragonflies on a variety of spatial scales. Mature dragonflies must be able to locate a variety of features in the habitat that are critical to survival and reproduction, includ- ing sites for breeding, foraging, roosting, and thermoregulating. In many species, these sites do not coincide in space. Because individuals may repeatedly use particular sites for different activities, they must learn both the locations of these sites and routes among them. Further evidence of spatial mem- ory in dragonflies is provided by their site specificity on a finer scale. Breeding males, for example, often are faithful not only to a particular area, but to a specific territory site within that area. Males appear to become faithful to a territory site through localization, a process during which they explore the site and develop a spatial map of the location of the territory and its resources. Males also respond to their interactions with other individuals, adjusting both their choice of territories and their space use within their territories to reflect those interactions. In eastern amberwing dragonflies ( Perithemis tenera ), males are not faithful to territories on which they have lost a fight with another male; in contrast, males are more likely to be faithful to territories on which they successfully mated than to territories on which they obtained no matings. Similarly, while on territories, male amberwings adjust their position in response to negative and positive interactions. They move away from the side of the territory from which neighbors most frequently intruded, and they move toward locations from which they pursued a female. Territorial amberwings thus modify their space use at both the territory and within-territory spatial scale in response to their social environment. Their responses are consistent with the hypothesis that they learn from their positive and negative experiences and adjust their future space use accordingly. Further study of spatial learning in dragonflies would greatly enhance studies of dragonflies’ behavior and ecology, and help us understand learning in general. Although dragonflies (Order Odonata) have been the subjects of a great deal of scientific research, relatively little has been published on learning in this taxon, despite the likely importance of learning for animals that are both highly predacious and highly mobile. Work with larval dragonflies has provided clear evidence of learning in foraging behavior, with individuals learning, for example, to avoid noxious prey (Rowe, 1994), to pursue more actively those prey types that they have successfully captured (Bergelson, 1985), and to adjust their behavior to compensate for injury in detecting and capturing prey (Abbott, 1941; Caillere, 1970). Larvae can also learn to recognize predation risk through experience with chemical cues (Chivers, Wisenden, & Smith, 1996; Wisenden, Chivers, & Smith, 1997), and adult males are known to learn to recognize potential mates when fe- males have more than one color pattern (Fincke, 2004; Miller & Fincke, 1999; Van Gossum, Stoks, & De Bruyn, 2001a, 2001b; Van Gossum, Stoks, Matthysen, Valck, & De Bruyn, 1999). Given the natural history and behavior of the dragon- flies, however, spatial learning must be one of dragonflies' most critical capabili- ties, and dragonflies must be capable of spatial learning on a variety of scales. Correspondence concerning this article should be addressed to Perri K. Eason, Department of Biol- ogy, University of Louisville, Kentucky 40292, U.S.A. ([email protected]). - 269 - In this paper we will focus on spatial learning in adult dragonflies, particu- larly as it relates to finding and using sites of reproduction. We will use the term “dragonfly” when referring in general to a member of the Order Odonata or when referring to a particular species in the suborder Anisoptera. We will use the term damselfly only when referring to a specific example of a member of the suborder Zygoptera. In the sections that follow, we first describe the different spatial scales commonly relevant to dragonflies and briefly review what is known about dragon- fly learning on each of these scales. We then discuss how learning might play a role in determining individuals’ location preferences at each scale level. Finally, we apply these ideas in a case study of the amberwing dragonfly, Perithemis ten- era . Spatial Learning Mature dragonflies must be able to locate a variety of features in the habi- tat that are critical to their survival and reproduction, and in most species, sites providing these features do not coincide in space. First, dragonflies in general have very specific requirements for breeding sites, which are most commonly located along streams or ponds. Males defending breeding territories, however, typically defend those territories for only part of each day (Alcock, 1987, 1989), and fe- males often visit the territories only when ready to mate and lay eggs (e.g., Hilton, 1984). Second, dragonflies need sites for foraging, preferably locations that have abundant arthropod prey. Because breeding areas typically have high densities of dragonflies, the best foraging sites for aggressive species may be at other locations, where foragers will have less interference and competition from conspecifics and where prey density may be higher (Baird & May, 2003). In many species, in fact, males feed little if at all while they are on their territories; in particular, males that spend relatively little time on their territory are less likely to forage there (Parr, 1983). Females, too, rarely forage on breeding territories, presumably due at least in part to interference by males seeking mates. Third, dragonflies typically use roosts, which are sites to which they retreat when light levels are low or when the weather conditions are unfavorable and which may be more than 1.5 km away from their breeding sites (reviewed in Corbet, 1999). Roosting may reduce preda- tion risk either through the formation of aggregations, which might reduce the risk for any one individual, or through the selection of roosting sites at which predation risk is lower than at the breeding sites. Finally, individuals in many species choose specific sites for thermoregulation, for example, by leaving a breeding site to perch in a sunnier location (Clausnitzer, 1998). Such ‘sun-flights’ are likely to be particu- larly common in the many species that breed in forested habitats, where oviposi- tion sites tend to be shaded. In most odonate species, then, adults must move among discrete locations that they use for different purposes. For all four of the types of locations mentioned above, there is evidence that individuals make more than one trip to a given site, suggesting that the animals learn the locations of the sites they use. For example, although few data are available for females, male odonates are commonly faithful to one or a few particular areas for reproduction. Substantial evidence for this is provided by numerous studies of marked individuals, which are often resighted at a - 270 - particular pond or section of a stream (e.g., Beukema, 2002; Clausnitzer, 1996, 1998; Koenig & Albano, 1987; reviewed in Corbet, 1999; Switzer, 1995). Dragon- flies appear to be less faithful to particular foraging areas than they are to breeding areas, and shifting foraging areas between days may be the norm, although too few species have been well studied to draw a firm conclusion. Nonetheless, within a given day individuals may forage in the same location for hours, and some indi- viduals return to the same foraging area over several days, suggesting again that they are capable of learning the location of a particular area (May & Baird, 2002). In addition, dragonflies appear to be able to learn the locations of foraging areas with high prey density. For example, individuals of some species regularly forage near areas containing beehives, and others appear to be able to locate swarms of flies and mosquitoes that persist over several days at the same site (Wright, 1945). In some species that have been carefully observed, individuals also appear to re- turn to the same areas for roosting (Grether & Switzer, 2000; Miller, 1989) and to the same areas for sunning (Clausnitzer, 1998). For example, Grether and Switzer (2000) found that a male rubyspot damselfly ( Hetaerina americana ) tended to re- turn to the same roosting aggregation night after night, but often shifted his roost location if he obtained a new territory in a different part of the stream. Dragonflies that have long commutes among the locations they frequent probably use both visual landmarks and a sun compass to navigate. Evidence for the latter comes from studies of long-distance migration; however, migrants also follow distinctive, linear features of the landscape, such as roads or stream (re- viewed by Corbet, 1999). Dragonflies with shorter commutes may rely primarily on “piloting” (i.e., using familiar landmarks and/or spatial memory to navigate). For example, careful observation revealed that a male traveling between his breed- ing site and a sun perch repeatedly used the same flight route, suggesting that he followed a learned route when commuting between the two locations (Clausnitzer, 1998). Few experimental studies have been performed to demonstrate that dragon- flies use landmarks and spatial memory for commuting. However, in one interest- ing study, Leucorrhinia duba males returned to a pond that had been covered by a cloth, and they even displayed reproductive behaviors there despite the absence of visible water (Sternberg, 1990, cited in Corbet, 1999). These males were probably using cues provided by the surrounding landscape to identify the site of their pond. Similarly, foraging dragonflies presumably relocate an insect swarm by learning the topography around the site of the swarm (Corbet, 1999).