Stage-Specific Behavioral Responses of Ageneotettix deorum (Orthoptera: Acrididae) in the Presence of Lycosid Spider Predators

Transcription

1 Journal of Insect Behavior, Vol. 16, No. 4, July 2003 ( C 2003) Stage-Specific Behavioral Responses of Ageneotettix deorum (Orthoptera: Acrididae) in the Presence of Lycosid Spider Predators Bradford J. Danner 1 and Anthony Joern 1,2 Accepted April 2, 2003; revised May 2, 2003 Grasshoppers must gather food while avoiding size-selective predation from other arthropods, especially spiders, potentially leading to a trade-off between foraging and defensive behaviors. This trade-off becomes less intense as prey grow larger and are less susceptible to arthropod predation. Activity budgets were constructed for three nymphal (third- to fifth- instar) and adult life cycle stages of Ageneotettix deorum, a common rangeland grasshopper, for three conditions of predation risk by lycosid spiders (spider absence, spider presence, and presence of a nonlethal, chelicerae-modified spider). In third and fourth instars, exposure to predators resulted in reduced feeding activity, increased time spent in antipredator and defensive behaviors, and reduced general activity compared to individuals not exposed to spiders. No significant shifts in behaviors were observed for fifth-instar nymphs and adult A. deorum in response to spider presence. Activity levels in functional spiders and chelicerae-modified spiders were statistically indistinguishable. KEY WORDS: grasshopper ecology; predator prey interaction; Ageneotettix deorum; Lycosid wolf spider; activity budgets. 1 School of Biological Sciences, University of Nebraska Lincoln, Lincoln, Nebraska To whom correspondence should be addressed at 348 Manter Hall, University of Nebraska Lincoln, Lincoln, Nebraska tjoern@unlserve.unl.edu. Fax: (402) /03/ /0 C 2003 Plenum Publishing Corporation

2 454 Danner and Joern INTRODUCTION While foraging, prey must balance feeding needs against those of predation risk (Lima and Dill 1990; Lima 1998a, b), interactions that are often determined by relative age or size relationships between the participants (Day et al., 2002). For arthropods, these dependencies are linked according to the coincidence of appropriate predator and prey life cycle stages. Immature insects must balance the acquisition of food required for growth against the risk of lethal predatory encounters (Houston and McNamara, 1990; Houson et al., 1993; Gotthard, 2000; Mangel and Stamps, 2001). Because of this tradeoff, foraging activities of prey may change in the presence of predators, leading to either lowered food intake rate or acceptance of lower-quality food under conditions of decreased exposure to predators (Lima and Dill, 1990; Rothley et al., 1997; Schmitz et al., 1997). Possible indirect life history outcomes resulting from predator-induced behavioral modification of prey may be decreased developmental rates (Rowe and Ludwig, 1991; Houston et al., 1993; Hutchinson et al., 1997), attainment of a lower than optimal size for a given life stage (Rowe and Ludwig, 1991), decreased reproductive performance during developmentally mature life stages (Fraser and Gilliam, 1992), or, ultimately, death from starvation. As prey outgrow size-based risk of predation, behavioral compensation in the presence of predators should no longer occur (Lima and Dill, 1990; Relyea and Werner, 1999). Predation has the potential to directly and indirectly affect lifetime fitness of grasshoppers (Joern, 1987; Joern and Gaines, 1990; Belovsky and Slade, 1993). Grasshoppers experience size-selective predation from a suite of consumers throughout their life cycle; smaller size is generally associated with higher susceptibility to aggressive arthropod predators (Cherrill and Begon, 1989; Schmitz et al., 1997; Schmitz, 1998; Oedekoven and Joern, 1998, 2000; Okuyama, 1999). Wandering wolf spiders (Lycosidae: Aranae) are often important predators of grasshopper nymphs (Beckerman et al., 1997; Rothley et al., 1997; Schmitz et al., 1997; Schmitz, 1998; Oedekoven and Joern, 1998, 2000; Okuyama, 1999), while adult grasshoppers from this system are at risk primarily to birds and robber flies (Diptera: Asilidae) (Joern and Rudd, 1982; Joern, 1988, 1992). In addition to directly consuming grasshopper nymphs (Oedekoven and Joern, 1998, 2000; Okuyama, 1999), lycosid spiders may also negatively affect prey by decreasing general activity, thus limiting food consumption (Beckerman et al., 1997; Schmitz et al., 1997; Rothley et al., 1997; Schmitz, 1998). Limited access to highly nutritious leaf material in the presence of spiders can reduce grasshopper fitness (Beckerman et al., 1997; Schmitz et al., 1997; Oedekoven and Joern, 2000). Additionally, a spider may interfere with a grasshopper s ability to thermoregulate properly, assuming that exposure

3 Grasshopper Behavioral Responses to Spiders 455 to direct sunlight may lead to increased exposure to predation risk (Kemp, 1986; Gillis and Smeigh, 1987; Lactin and Johnson, 1998). While predation clearly affects grasshopper life histories, adverse effects of predation risk can be diminished through cryptic morphology and behavior that reduces detection, such as active escape or avoidance, and altered activity cycles and microhabitat use that does not correspond to the primary periods and sites of spider activity (Otte and Joern, 1977; Lawton and Strong, 1981; Jeffries and Lawton, 1984; Holt and Lawton, 1994; Schmitz et al., 1997). Such behaviorally mediated effects serve to reduce the effectiveness of predators but may also reduce the grasshopper s nutrient and energy budget by limiting consumption and digestion, thus affecting underlying resource allocation processes to key life history needs (maintenance, growth, reproduction, storage) (Wooton, 1994; Relyea and Werner, 1999). Past studies evaluated indirect effects of spider predation risk by modifying the chelicerae to eliminate killing ability without altering hunting activity (Okuyama, 1999; Schmitz et al., 1997). We used this technique to examine multiple grasshopper behaviors in response to the presence of a predator and relate results to probable impacts on fitness that may affect individual performance or population dynamics of rangeland grasshoppers (Johnson and Mundel, 1987; Joern and Gaines, 1990). We investigated the hypothesis that individuals susceptible to spider predation will alter time budgets in order to minimize exposure to predators by reducing feeding to assume more defensive or vigilant behaviors. We predicted that behavioral repertoires of younger, more susceptible grasshoppers would exhibit greater variation in response to the presence of spiders in comparison to older life stages. Additionally, we determined whether disabling a spider s chelicerae and hence feeding ability would affect the behavioral repertoire of immature grasshoppers in the same manner that a normal spider would. We also assessed whether activity levels differed between spiders capable of normal hunting and those with modified chelicerae. MATERIALS AND METHODS Study Site This study was conducted during June and July of 2002 at Cedar Point Biological Station (Keith County, NE), located approximately 2 km south of Lake Ogallala. Grasses intermixed with small open areas dominated ground cover, while some forbs were present. Common arthropod predators at this site were lycosid spiders and robber flies (Diptera: Asilidae). Spiders were easily caught on site using pitfall trapping and hand capture in random

4 456 Danner and Joern encounters. We used Schizocosa spp. as our experimental predator, as it was the predominant lycosid spider found at this site. All spiders used for experimental treatments had a cephalothorax abdomen length greater than 12 mm and less than 18 mm, a size class fully capable of subduing immature A. deorum (Oedekoven and Joern, 1998). All spiders lived over the course of the experiment and were released fully capable of foraging. Experimental Design Cylindrical cages (18-cm radius, 30-cm height) were constructed of 3- mm-mesh hardware cloth and attached to a wooden stake driven into the ground to insure stability. Forty-eight cages constructed in this manner were arrayed in 16 groups of three. Cages were placed over patches dominated by grama grasses (Bouteloua spp.), the primary host plants for Ageneotettix deorum (Joern, 1985). At the time these experiments were conducted, all the vegetation at this site was less than 30 cm tall, and vertical restriction of grasshopper movement was not an issue. Evidence suggests that the area enclosed by our cages falls within the levels of A. deorum daily movement while searching for food (Joern, 1982; Narisu et al., 1999). In the natural spider cages, a spider with normal, unaltered chelicerae was placed in the cage. In the modified spider cages, a drop of softened beeswax was placed on the chelicerae of the spider to prohibit feeding. Following trials, wax was removed and spiders fed. This method has been successfully employed in other studies to elicit behavioral responses of grasshoppers (Schmitz et al., 1997; Okuyama, 1999). After stocking cages with spiders, grasshoppers were caught and arbitrarily placed in cages. Behavioral observations were recorded using scan sampling after an acclimation period of 24 h (Martin and Bateson, 1986). Groups of three cages in close proximity were watched for a period of 1 h. A behavioral observation was recorded for each cage every 20 s. Because of the relatively small size of cages, both grasshopper and spider participants were readily detected during each sample scan. Approximately 20 min of behavioral observations was made for each grasshopper and spider. Eight 1-h periods were conducted between 0800 and 1700 h, when A. deorum is typically active. The experiment was then repeated the following day in the same manner using different grasshoppers and spiders, yielding 16 replicates of each treatment. This protocol was employed using three immature instars and adults as they became available. Six grasshopper behavioral categories were scored and are listed in Table II. Jumping and Walking both include movement but differ as indicated. Perching is a behavioral category where the individual is quiescent

5 Grasshopper Behavioral Responses to Spiders 457 and sitting on substrate in open view of the observer. The actual selection of perch relative to incoming sun and/or nature of the background facilitating crypsis may be important, but these factors are not included in the categorization. A behavior was scored as concealment if the grasshopper actually positioned itself under some naturally occurring cover (e.g., a leaf) and did not move. Feeding indicates that the animal was actively consuming leaf material. The category Cleaning represents active movement of the legs along different body parts, particularly the antennae and mouthparts. Spider activity was explicitly defined as movement in any direction during an observation or movement to a different location since the previous observation. Statistical Analyses Overall differences in time budget profiles spider treatments were assessed using multivariate analysis of variance (MANOVA) to accommodate the lack of independence between behavioral activities of individual grasshoppers. Separate ANOV As were conducted on individual behavioral categories to determine differences. Specific comparisons between treatment levels for each behavior were conducted using a Tukey s adjustment in order to avoid increasing the possibility of a Type I error given the large number of comparisons. Observations of spider activity were assessed within life stage using separate one-way ANOVAs. RESULTS Spider Activity Spider activity measured as the number of active observations during a 1-h time period is shown in Table I. The activity of modified and natural spiders was not significantly different (P 0.05) across the four prey life stages observed in this experiment. In addition to walking and climbing, spiders were observed to sometimes attack resident grasshoppers. One successful attack was recorded while we were observing fourth-instar grasshoppers. Since the predatory event occurred during the first half of the observational trial, this replicate was excluded from the remainder of the analysis. Grasshopper Activity Budgets During the third and fourth instars, behavioral activity budgets of grasshoppers were significantly affected by the presence of a spider (Table II). The effects were slightly more pronounced for third-instar nymphs (Wilks

6 458 Danner and Joern Table I. Mean (±1 S ) Number of Active Observations Recorded for Spiders During the 1-h Experimental Periods a Third instar Fourth instar Fifth instar Adult Modified spider Number of individuals b Active observations (3.14) (4.96) (4.09) (2.67) Natural spider Number of individuals c Active observations (2.69) (4.85) (4.21) (2.87) Planned contrast F P a Spider activity was defined as movement in any direction during an observation or movement to a different location since the previous observation. Results of separate one-way ANOVA per grasshopper instar tested are given. b One replicate during this period was thrown out because the grasshopper was able to escape. c One replicate during this period was thrown out because the spider was observed to directly consume the experimental grasshopper in the cage. λ = 0.06, F = 24.4, df = 10,82, P < 0.001) in comparison to fourth-instar nymphs (Wilks λ = 0.18, F = 10.8, df = 10, 80, P < 0.001). No significant response was detected for fifth-instar nymphs (Wilks λ = 0.93, F = 0.37, df = 8,84, P = 0.93) and adults (Wilks λ = 0.74, F = 1.69, df = 8,82, P = 0.11). Planned contrasts for specific behaviors revealed no significant differences between the activities of grasshoppers in the two spider treatments ( P > 0.05) for most behaviors (19 of 22 possible compansons). Exceptions included Concealment during the third instar ( P = 0.011), Jumping during the fourth instar (P = 0.004), and Jumping during the adult stage ( P = 0.016) (Table II). Significant grasshopper behavior responses to the presence or absence of spiders were revealed (P < 0.05) for all categories during the third instar, except Concealment. During the fourth instar, behaviors of grasshoppers observed in the absence of a spider all differed from those in the presence of a spider (P < 0.05), except for the Cleaning and Feeding categories ( P 0.05). No differences in bahavioral time budgets were observed between spider treatments for the fifth instar or adult life stage (Table II). Grasshoppers spent significantly less time foraging while spiders were present in cages during the third instar (Fig. 1). Additionally, many more jumps were observed per grasshopper when caged with a predator, for all immature instars (Table II). As grasshoppers develop, they become larger and less susceptible to spider predation and may not be required to jump as often to escape potential predatory events.

7 Grasshopper Behavioral Responses to Spiders 459 Table II. Mean (±1 S ) Number of Observations Within Specific Behavioral Categories Recorded for Grasshoppers During the 1-h Experimental Periods, Calculated Using the 16 Replicates Within Each Treatment per Instar Tested a Jumping Walking Perching Concealment Cleaning Feeding Third instars No spider 0.13 (0.13) (1.88) (0.86) 1.38 (0.50) 3.93 (0.41) 3.63 (0.78) Modified spider 4.25 (0.51) (0.94) (1.69) 6.63 (1.03) 0.19 (0.10) 0.13 (0.09) Natural spider 3.75 (0.57) (0.98) (0.99) 3.00 (0.91) 0.19 (0.19) 0.06 (0.06) Fourth instars No spider 0.31 (0.18) (1.66) (1.82) b 2.00 (0.37) 3.94 (0.72) Modified spider 6.50 (0.70) (1.47) (1.63) 3.12 (1.02) 2.00 (0.45) 4.44 (0.79) Natural spider 3.93 (0.56) (1.38) (0.66) 3.47 (1.01) 2.73 (0.69) 4013 (1.00) Fifth instars No spider 1.21 (0.37) (0.68) (1.15) 5.88 (0.70) (0.69) Modified spider 1.25 (0.39) (0.69) (1.62) 5.38 (0.49) (1.03) Natural spider 1.50 (0.42) (0.96) (1.54) 5.63 (0.74) (0.71) Adults No spider 0.69 (0.24) (0.76) (1.62) 7.31 (0.74) (1.24) Modified spider a 8.60 (0.90) (1.41) 8.27 (0.78) (0.99) Natural spider 0.88 (0.27) 8.25 (0.68) (1.19) 8.63 (0.61) (1.05) a According to our definitions, Concealment could be considered a subset of the Perching category, where the grasshopper is visibly observed to remain still underneath naturally occurring vegetation. b No observation within this behavioral category was recorded among the 16 replicates.

8 460 Danner and Joern Fig. 1. Estimate of time spent feeding by dividing the mean numbre of feeding observation recorded per treatment by the 60-min time period the grasshoppers were observed. Bars represent one standard error. DISCUSSION While foraging, herbivores must balance searching, consumption, and digestion of quality host plant food while minimizing the likelihood of detection and capture by predators (Werner and Gilliam, 1984; McNamara and Houston, 1987; Mangel and Clark, 1986; Houston et al., 1993). Grasshoppers minimize detection by predators through vigilance, and the level of vigilance should vary in response to the recent presence or absence of predators, coupled to the relative risk of being attacked (Rothley et al., 1997). Vigilance and foraging present competing demands such that time spent in one activity necessarily reduces time available for the other. For example, feeding activity and consumption of high-quality grass were limited by predation risk from lycosid spiders in the grasshopper Melanoplus femurrubrum (Rothley et al., 1997; Schmitz et al., 1997), demonstrating that grasshoppers have the ability to balance multiple demands (Rothley et al., 1997).

9 Grasshopper Behavioral Responses to Spiders 461 As a common prey item of both wandering spiders (Oedekoven and Joern, 1998, 2000) and birds (Joern, 1992), we expected that A. deorum must routinely balance feeding and predator avoidance. Here, we tested the prediction that activity budgets of younger, more susceptible nymphs will be influenced to a greater degree by the presence of spiders than will older, larger individuals (Oedekoven and Joern, 1988). Specifically, we expected increased contribution by activities facilitating vigilance while decreasing other activities, such as feeding when predators were present. Results were consistent with predictions. In the presence of spiders, younger A. deorum significantly reduced the time spent walking, feeding, and cleaning while increasing the proportion of time in quiescent perching, sometimes positioning themselves under vegetation and litter (concealment). A significant proportion of time in quiescent activity, presumably in vigilant activities and possibly thermoregulation (facilitating digestion and active escape if needed), has been noted for related species (Joern et al., 1986; Joern, 1987). Jumping was more common during younger stages in the presence of spiders, presumably triggered by spider movement. Time budget differences among spider treatments were not observed in fifth-instar nymphs or adults, stages that do not typically experience a significant risk to spiders naturally (Oedekoven and Joern, 1998). Again, this pattern is consistent with predictions. Observations were recorded throughout the day, integrating daily variation in environmental conditions, especially temperature. For obvious biological reasons, field trials for different developmental stages were performed separately and under potentially different conditions reflecting natural seasonal progression. Specifically, daytime temperatures were hotter during trials of adult A. deorum in comparison to immature life cycle stages. Because spiders are less active at higher temperatures (Schmitz et al., 1997), decreased spider activity in later trials may account in part for diminished differences in grasshopper responses at later stages. However, conditions and seasonal shifts in temperature were normal for this site, indicating that typical natural responses were observed. The presence of spiders clearly influences A. deorum, as seen by the shift in time budgets. Reduced time spent feeding (and increased time spent perching) negatively alters nutritional budgets by reducing the amount of quality food eaten per day (Rothley et al., 1997), potentially affecting subsequent developmental rates, survival, reproduction, and possibly species interactions with potential competitors (Chase, 1996a, b; Werner and Anholt, 1996). Moreover, decreased food intake may lower individual quality (e.g., absolute size, resource reserves) relative to individuals that encounter spiders less (Oedekoven and Joern, 2000). Whether older stages can compensate for early relative losses in food intake is unknown.

10 462 Danner and Joern It is important to recognize that larger (older) A. deorum do not react to spiders with a shift in foraging activity (Fig. 1). Evidence from other studies with this grasshopper suggest that negative, nonlethal impacts of spider predation can cause a reduced growth rate, partially mediated through food quality, and delayed reproduction (Danner, 2002). Additionally, behavioral responses to important predators of adult grasshoppers, such as birds, may also occur, but these were not examined (Joern and Gaines, 1990). Shifts in prey behavioral time budgets in response to predator presence may influence a number of important ecological interactions elicited by these insect herbivores, such as intra- and interspecific competition (Werner and Gilliam, 1984; Chase, 1996a, b), nutrient cycling in grasslands (van Hook, 1971), and population densities the following year (Joern and Gaines, 1990). The interaction between wolf spider predators and their immature grasshopper prey provides an example where behavioral modification, specifically reduced performance during developmentally immature instars, may have significant implications at population, community, and ecosystem levels. ACKNOWLEDGMENTS We greatly appreciate logistical support provided by Cedar Point Biological Station (UNL). We would like to thank John Holtz, Svata Louda, Os Schmitz, Kristal Stoner, and an anonymous reviewer for critical comments on previous versions of the manuscript. Discussions with Al Kamil were very helpful. Research was supported by NSF Grant and supplemented by funds provided by the Initiative for Ecological and Evolutionary Analysis and the School of Biological Sciences (University of Nebraska Lincoln). REFERENCES Beckerman, A. P., Uriarte, M., and Schmitz, O. J. (1997). Experimental evidence for a behaviormediated trophic cascade in a terrestrial food chain. Proc. Natl. Acad. Sci. USA 94: Belovsky, G. E., and Slade, J. B. (1993). The role of vertebrate and invertebrate predators in a grasshopper community. Oikos 68: Chase, J. M. (1996a). Differential competitive interactions and the included niche: An experimental analysis with grasshoppers. Oikos 76: Chase, J. M. (1996b). Varying resource abundances and competitive dynamics. Am. Nat. 147: Cherrill, A. J., and Begon, M. (1989). Predation on grasshoppers by spiders in sand dune grasslands. Entomol. Exp. Appl. 50: Danner, B. J. (2002). Performance of Ageneotettix deorum (Orthoptera: Acrididae) in Response to Lycosid Spider Predation risk and Food Quality, Thesis. University of Nebraska, Lincoln. Day, T., Abrams, P. A., and Chase, J. M. (2002). The role of size-specific predation in the evolution and diversification of prey life histories. Evolution 56:

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