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Journal of Insect Behavior, Vol. 16, No. 4, July 2003 (°
Stage-Specific Behavioral Responses of Ageneotettix
deorum (Orthoptera: Acrididae) in the Presence of
Lycosid Spider Predators
Bradford J. Danner1 and Anthony Joern1,2
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.
1School
of Biological Sciences, University of Nebraska—Lincoln, Lincoln, Nebraska 685880118.
2To whom correspondence should be addressed at 348 Manter Hall, University of Nebraska—
Lincoln, Lincoln, Nebraska 68588-0118. e-mail: tjoern@unlserve.unl.edu. Fax: (402) 472-2083.
453
C 2003 Plenum Publishing Corporation
0892-7553/03/0700-0453/0 °
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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
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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
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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 3mm-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
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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 À 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’
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Table I. Mean (±1 S1) Number of “Active” Observations Recorded for Spiders During the
1-h Experimental Periodsa
Modified spider
Number of individuals
“Active” observations
Natural spider
Number of individuals
“Active” observations
Planned contrast
F
P
Third instar
Fourth instar
Fifth instar
Adult
16
15.56 (3.14)
16
13.81 (4.96)
16
13.31 (4.09)
15b
10.87 (2.67)
16
15.94 (2.69)
15c
13.67 (4.85)
16
12.19 (4.21)
16
11.13 (2.87)
0.13
0.7195
0.01
0.9346
0.59
0.4497
0.07
0.7975
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.
during this period was thrown out because the grasshopper was able to escape.
during this period was thrown out because the spider was observed to directly
consume the experimental grasshopper in the cage.
b One replicate
c One replicate
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 À 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.
25.94 (1.88)
11.69 (0.94)
13.88 (0.98)
31.00 (1.66)
14.18 (1.47)
14.27 (1.38)
10.81 (0.68)
10.69 (0.69)
10.25 (0.96)
10.25 (0.76)
8.60 (0.90)
8.25 (0.68)
0.13 (0.13)
4.25 (0.51)
3.75 (0.57)
0.31 (0.18)
6.50 (0.70)
3.93 (0.56)
1.21 (0.37)
1.25 (0.39)
1.50 (0.42)
0.69 (0.24)
a
0.88 (0.27)
—
—
—
7.31 (0.74)
8.27 (0.78)
8.63 (0.61)
5.88 (0.70)
5.38 (0.49)
5.63 (0.74)
2.00 (0.37)
2.00 (0.45)
2.73 (0.69)
—b
3.12 (1.02)
3.47 (1.01)
—
—
—
3.93 (0.41)
0.19 (0.10)
0.19 (0.19)
Cleaning
1.38 (0.50)
6.63 (1.03)
3.00 (0.91)
Concealment
11.88 (1.24)
13.20 (0.99)
12.69 (1.05)
10.25 (0.69)
10.38 (1.03)
11.69 (0.71)
3.94 (0.72)
4.44 (0.79)
4013 (1.00)
3.63 (0.78)
0.13 (0.09)
0.06 (0.06)
Feeding
to remain still underneath naturally occurring vegetation.
observation within this behavioral category was recorded among the 16 replicates.
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29.88 (1.62)
29.93 (1.41)
29.56 (1.19)
31.75 (1.15)
32.31 (1.62)
30.94 (1.54)
22.75 (1.82)
29.75 (1.63)
31.47 (0.66)
25.00 (0.86)
37.12 (1.69)
39.13 (0.99)
Perching
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a According to our definitions, Concealment could be considered a subset of the Perching category, where the grasshopper is visibly observed
Third instars
No spider
Modified spider
Natural spider
Fourth instars
No spider
Modified spider
Natural spider
Fifth instars
No spider
Modified spider
Natural spider
Adults
No spider
Modified spider
Natural spider
Walking
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Table II. Mean (±1 S1) 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 Testeda
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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).
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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.
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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 0087253 and supplemented
by funds provided by the Initiative for Ecological and Evolutionary Analysis
and the School of Biological Sciences (University of Nebraska—Lincoln).
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