Behavioral Ecology Vol. 13 No. 3: 386-392
© 2002 International Society for Behavioral Ecology
Fitness costs and benefits of antipredator behavior mediated by chemotactile cues in the wolf spider Pardosa milvina (Araneae: Lycosidae)
a Department of Zoology, Miami University, Oxford, OH 45056, USA b Department of Zoology, Miami University, Hamilton, OH 45011, USA
Address correspondence to M.H. Persons, who is now at the Department of Biology, Susquehanna University, Selinsgrove, PA 17870, USA. E-mail: persons{at}susqu.edu .
Received 15 December 2000; revised 7 June 2001; accepted 7 August 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDISCUSSIONREFERENCES |
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Animals may exhibit a variety of defensive behaviors in the presence of indirect predator cues. Such behavior offers immediate fitness benefits but may also incur substantial foraging and reproductive costs. We measured shifts in space use (vertical climbing) by the wolf spider Pardosa milvina induced by chemotactile cues (silk and excreta) from a co-occurring predatory wolf spider Hogna helluo. We then measured foraging and reproductive costs, as well as survival benefits, of this behavior. For 2 weeks, we maintained mated adult female Pardosa in plastic containers with one of three treated peat moss substrates: a container previously occupied by a conspecific for 3 days, a container previously occupied by an adult Hogna for 3 days, and a container devoid of either cue (control). We measured prey capture efficiency, body condition, egg sac production, egg sac weight, and egg number for individuals in each treatment. We also counted the number of Pardosa that survived and exhibited climbing behavior in the presence of a live Hogna with and without silk and excreta cues. Pardosa climbed container walls significantly more often in the presence of Hogna silk and excreta relative to other treatments. Pardosa exposed to Hogna cues coupled with live Hogna survived significantly longer than spiders that had no predator cues available. Pardosa placed in containers with Hogna cues, but no Hogna, lost weight more quickly, ate fewer prey, were in poorer body condition, produced lighter egg sacs, and produced fewer eggs than spiders in control or conspecific treatments.
Key words: antipredator behavior, chemotactile cues, Hogna helluo, Lycosidae, Pardosa milvina, reproductive costs, survival benefits, wolf spiders.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONREFERENCES |
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Prey often exhibit behavioral adaptations to avoid predation such as avoidance (Brown et al., 1995
;
Gore, 1966), reduced activity
(Holomuzki and Short, 1990;
Malmqvist, 1992), cover
seeking (Kats et al., 1988;
Wahle, 1992), or increased
vigilance (Sweitzer and Berger,
1992). Early predator detection is often critical for effective
use of these tactics. Therefore, many prey have evolved the ability to detect
a variety of metabolic by-products associated with the presence of predators
and exhibit appropriate behavior even in the absence of the predator itself
(reviewed in Chivers and Smith,
1998; Kats and Dill,
1998). Preemptive antipredator tactics may incur substantial
fitness costs such as reduced foraging success (reviewed in
Lima, 1998;
Lima and Dill, 1990) or
impaired reproduction (reviewed in
Magnhagen, 1991;
Kats and Dill, 1998;
Repka et al., 1994). These
costs may, in turn, translate into a number of life-history changes
(Crowl and Covich, 1990) such
as delayed development, slower growth
(Barry, 1994;
Spitze, 1992) or postponed
reproduction (Koskela and Ylönen,
1995; Ylönen and
Ronkainen, 1994).
Despite an extensive body of literature on prey responses to indirect
predator cues, few such studies exist among terrestrial arthropods
(Kats and Dill, 1998;
Persons et al., 2001;
Venzon et al., 2000), and even
fewer studies document the costs incurred by arthropods exhibiting chemical or
tactile-mediated defensive behavior
(Grostal and Dicke, 1999;
Hoffmeister and Roitberg,
1997).
Wolf spiders provide an interesting taxon to examine indirectly mediated
predator-prey interactions because, in addition to excreta, they also leave a
silk dragline behind them while moving through the environment. Because wolf
spiders are common prey as well as predators of other species of wolf spider
(Persons and Rypstra, 2000),
they may be especially likely and able to detect and respond to spider silk
and excreta cues. The wolf spider species Hogna helluo (Walckenaer)
(Araneae: Lycosidae) and Pardosa milvina (Hentz) (Araneae: Lycosidae)
are syntopic intraguild predators. Both species live in early successional
habitats and are often the two most abundant cursorial spiders in agricultural
systems of the eastern and central United States
(Dondale and Redner, 1990;
Marshall and Rypstra, 1999;
Young and Edwards, 1990).
Neither species constructs a web, and both are typically found on the soil
surface or residing on low-lying vegetation, where they feed on a wide variety
of ground-dwelling arthropods including cursorial spiders, collembola, and
crickets (Persons et al., personal observations). Hogna is a large
wolf spider (adult female ca. 300-800 mg) and has frequently been observed to
prey on the much smaller Pardosa (ca. 20 mg)
(Persons et al., 2001).
Pardosa exhibits a variety of defensive tactics when exposed to silk
and excreta cues produced by Hogna, including prolonged periods of
immobility, reduced walking speeds, and substrate avoidance
(Persons et al., 2001). These
behaviors minimize predation in the presence of Hogna
(Persons et al., 2001).
Pardosa has also been anecdotally observed to shift space use by
climbing vertical surfaces when exposed to Hogna silk and excreta.
Behavioral responses may be mediated by chemicals found within silk and
excreta, localized structural changes to the substratum, or tactile
information embedded within the predator cues. For this reason, we refer to
behaviorally relevant information found in silk and excreta as chemotactile
cues. To date, the potential direct and indirect fitness costs of
chemotactile-mediated antipredator behavior has not been experimentally
demonstrated in any species of spider.
Female Pardosa, like all lycosids, attach their egg sacs to their
spinnerets. Egg sacs are energetically expensive to produce, constituting more
than 30% of the mass of the spider (Edgar,
1971; Marshall and Gittleman,
1994). Therefore, any behavior that reduces foraging success or
results in less energy being available for reproduction should result in a
reduction in egg number or egg mass, or a delay in the timing of egg sac
production.
Here we addressed possible foraging and reproductive costs as well as survival benefits associated with a shift in space use (vertical climbing) by Pardosa when exposed to silk and excreta produced by Hogna. We tested the five hypotheses: (1) Pardosa should shift their locations to vertical surfaces (climbing movement) in the presence of silk and excreta cues from Hogna compared to conspecific silk and excreta or substrates lacking either cue; (2) shifts in space use should result in either reduced foraging success and/or increased energy expenditure as measured by spider body condition; (3) Pardosa should reduce feeding in the presence of cues from Hogna compared to conspecific cues; (4) long-term exposure to predator chemotactile cues should delayed reproduction and reduce reproductive output; and (5) vertical climbing should increase survival in the presence of live Hogna compared to spiders that do not exhibit this behavior.
General spider collection and maintenance
For all experiments we collected adult female Pardosa with egg
sacs from soybean fields at Miami University's Ecology Research Center
(Oxford, Butler County, Ohio, USA) in August 1998. Egg sacs were removed from
females within 48 h of any experiment unless otherwise indicated. Adult female
Hogna with spiderlings or egg sacs were collected from the same
soybean fields in August 1997, and their offspring were raised in the lab and
used as experimental predators or predator stimuli for all experiments.
Pardosa were maintained in 5.5 cm high x 5.5 cm diam containers
with a 2-cm layer of moistened peat moss covering the bottom. Each container
was covered with a clear plastic lid. Hogna were maintained in 8 cm
high x 12 cm diam white plastic cups with clear lids and also had a 2 cm
deep layer of moistened peat moss provided as a source of water and burrowing
substrate. Both species were maintained on a diet of domestic house crickets
(Acheta domesticus).
Experiment 1: measuring behavioral changes and fitness consequences
of Pardosa exposure to Hogna cues
Methods
We measured shifts in space use of mated adult female Pardosa when
exposed to containers with peat moss substrates previously occupied by one of
the following: an adult female Hogna helluo, a conspecific female
Pardosa, or a substrate lacking either cue. Over a 2-week period, we
quantified the following for each Pardosa within each peat moss
treatment: changes in body condition (morphometric measure of weight loss
scaled to body size), latency to produce an egg sac, number of egg sacs
produced, egg sac weight, and egg number per egg sac. Additionally,
Pardosa were observed either on the side or bottom of the container,
and we used this as our behavioral response variable across each peat moss
treatment.
Peat moss stimulus preparation. All test Pardosa were randomly assigned among containers with three treatment groups of moistened peat moss (n = 25/treatment): (1) control, containers devoid of any spider cues; (2) conspecific cues, containers previously occupied for 3 days by a mated adult female; and (3) predator cues, containers previously occupied by an adult female Hogna for 3 days. Each treatment container consisted of a 12 cm diam x 8 cm high white plastic cup with a clear lid. Before adding peat moss, all plastic cups were rinsed with 95% ethanol to remove any residual odor cues from prior use. We then placed 2 cm of commercially obtained moist peat moss in the bottom of each container. For containers requiring a stimulus, a single Pardosa or Hogna was satiated with crickets during a 24-h period, then introduced into each cup. All stimulus spiders were maintained in the cup without food for 3 days and subsequently removed. A test Pardosa was introduced into each of the three peat moss treatment containers (control, Pardosa cues, or Hogna cues). A different individual Hogna and Pardosa were used for each container. Every 4 days, a new set of peat moss containers was set up to maintain fresh cues for each treatment group. Immediately after transfers to new containers, test spiders were fed to satiation through ad libitum feeding within the treatment containers. Thus spiders were transferred to a new container with 3-day-old cues every 4 days and fed to excess with additional prey added every 4 days (3 times during the 14-day test period). All spiders were maintained in environmental chambers with a 13:11h light:dark photoregimen at stable humidity (50-60%) and temperature (22-25°C).
Measurement of behavior, body condition, and egg sac production.
After the initial 4 days within each treatment, but before the first feeding
within the stimulus containers, we measured body condition (a size-independent
measure of nutritional state) for each test Pardosa (described in
Jakob et al., 1996).
Cephalothorax width and abdomen width were measured with dial calipers. Both
measures were taken at the greatest width for both cephalothorax and abdomen.
We used cephalothorax width as a measure of spider body size because it
remains constant with food intake within an instar
(Hagstrum, 1971;
Jakob et al., 1996). Abdomen
width increases as a function of feeding and was used as an index of body
condition.
Within each treatment group, the location of the spider—on the substrate or on the side of the container—was noted, and the presence or absence of an egg sac was recorded. A spider was recorded as being on the side of the container only if all eight legs were in contact with the wall and none with the substrate. We recorded spider location three times daily at 0800, 1200, and 2100 h. Environmental chamber lighting was set on a timer. Morning recordings were completed 30 min before artificial daylight and evening recordings were recorded 30 min after artificial nightfall. Morning and evening measurements were taken using a 15-watt flashlight as the sole light source. Once egg sacs had been deposited, the spider and egg sac were removed and weighed separately on an analytical balance and then placed in 70% alcohol so that the number of eggs could be determined at a later date. We collected spiders producing egg sacs during a 14-day period, after which point the experiment was terminated. Measurement of climbing behavior was discontinued after 8 days due to a reduction in sample size from spiders producing egg sacs.
Statistical analysis. Significant differences in climbing behavior for each chemotactile cue treatment were determined with a chi-square contingency table for each time period immediately following replacement of the substrate (the mornings of day 1, day 4, and day 8). We determined differences in spider abdomen width (body condition), egg sac mass, and egg number within each treatment using one-way ANOVAs and Tukey post-hoc comparison of means tests. Data were natural-log transformed to conform to ANOVA assumptions of normality when necessary. We compared differences in the number of individuals producing an egg sac within each treatment using a chi-square two-by-three contingency table. We used failure-time analysis using the Kaplan-Meier product limit estimator to compare differences in the median time to produce an egg sac, and we tested for a significant treatment effect and then compared the distribution of time to egg sac production using the log-rank (Mantel-Cox) test.
Results
Pardosa milvina exhibited significant differences in climbing
behavior across the three treatment groups for each time period tested
(Figure 1). Spiders spent
significantly more time on the sides of the containers in the presence of
Hogna cues than either the blank control treatment or the conspecific
treatment (Figure 1), and this
behavior appeared to continue over much of the 8-day recording period.
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We compared cephalothorax width of spiders across treatment groups to test
for the possibility that spiders differed in body size across groups by
chance. Spiders were not significantly different in cephalothorax width across
treatments (ANOVA, F2,71 = 0.39, p =.68),
demonstrating that body size was not significantly different across
treatments. Therefore, we used abdomen width alone rather than cephalothorax
width to abdomen width ratio as an index for body condition
(Jakob et al., 1996). After
being maintained for 4 days, Pardosa exhibited significant
differences in abdomen width between treatments
(Table 1). Because spiders were
not significantly different in cephalothorax width across treatments, this
indicates a significant difference in body condition between treatments
(Table 1). Tukey post-hoc
comparison of means test indicated that Pardosa maintained in the
Hogna cue treatment had significantly smaller abdomens than either
conspecific or control treatments (Table
1).
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There was no significant difference in the number of egg sacs produced
across treatment groups (
2 = 3.571, p =.167). Spiders
maintained in the Hogna cue treatment produced 15 egg sacs compared
to 18 and 21 for control and Pardosa treatments, respectively. There
was also no significant difference in the median time to produce an egg sac
across treatment groups (Mantel-Cox test for time to egg sac production,
2 = 1.264, df = 2, p =.5316; median = 12.00 ±
0.518 days for control treatment, 11.00 ± 0.414 days for
Pardosa treatment, and 11.00 ± q1.861 days for the
Hogna treatment). However, we did find significant differences in
mean egg sac weight between treatments
(Table 1), with spiders from
the Hogna treatment producing significantly lighter egg sacs than
spiders in the other two treatment groups
(Table 1). Pardosa
maintained in containers with Hogna cues also produced significantly
fewer eggs per egg sac than individuals from either of the other treatments
(Table 1).
Experiment 2: effects of perceived predation risk on feeding
behavior
Methods
Experiment 1 demonstrated that Pardosa lost weight significantly
faster in the presence of Hogna cues than conspecific cues or blank
controls. However, we were uncertain if differences in egg sac mass and egg
number were due to differences in the rate of weight loss alone or if
Pardosa also captured less prey in containers with Hogna
cues compared to the other treatments. Therefore, we examined the effect of
Hogna cues versus Pardosa cues on the feeding behavior of
Pardosa.
Stimulus preparation. We compared the number of prey consumed in 1.5 h by Pardosa in containers that had been previously occupied by either a Hogna or a conspecific (n = 13/treatment). Spiders were placed in opaque, colorless plastic food-service containers (5 cm high x 9 cm diam) with a 1 cm peat moss substratum. Hogna and Pardosa were fed crickets of an appropriate size once weekly before use in the experiment. The Pardosa were satiated, then fasted for 5 days before testing. To reduce variation in the production of Hogna and Pardosa excreta and silk, spiders to be used as stimuli for both treatments were sated with crickets 24 h before being placed in the containers. We introduced a single Hogna or Pardosa into the plastic container with a moistened peat moss substratum for 12 h. After 12 h we removed these spiders and placed a single test Pardosa into each container.
Measurement of feeding behavior and statistics. Five minutes after
Pardosa were introduced, five vestigial-winged fruit flies
(Drosophila melanogaster) were given to each spider. We then counted
the number of flies consumed by each spider after 1.5 h. We compared the
proportion of flies eaten between the two stimulus treatments (i.e.,
Hogna versus conspecific) using logistic regression with an indicator
variable. This type of procedure is analogous to doing an ANOVA using the
proper error distribution for data which consist of the number of
successes/number of trials (Collet,
1991; Stokes et al.,
1995). To verify that the number of prey killed was correlated
with prey biomass consumed, we also tested for a change in the nutritional
status of the test Pardosa by comparing body condition before and
after the experiment. Because abdomen width is an indicator of recent foraging
success (Jakob et al., 1996),
we measured abdomen width of each spider before and after the experiment and
calculated the change in width (width after — width before = change in
abdomen width). We then compared the changes in abdomen width between
treatment groups using a t test.
Results
Pardosa in containers that previously contained Hogna
consumed fewer fruit flies than did spiders in containers that previously
contained Pardosa (Table
1). Pardosa placed in containers with conspecific cues
not only killed more fruit flies, but also consumed more prey biomass, as
evidenced by an increase in abdomen width. The change in mean abdomen width
was greater for spiders in containers previously occupied by Pardosa
compared to abdomen width changes of spiders in containers previously occupied
by Hogna (Table
1).
Experiment 3: survival value of predator chemical cue detection and
climbing behavior
Methods
Because Pardosa behavior in the presence of Hogna cues is
sufficient to induce weight loss, reduce feeding efficiency, reduce prey
capture, and affect reproductive output, we were interested in the possible
immediate survival benefits of such behavior. We tested the survival of
Pardosa exposed to the risk of predation by Hogna with and
without substratum-borne cues from Hogna and also measured survival
of Pardosa that exhibited climbing behavior versus those spiders that
did not. We collected and maintained 60 adult female Pardosa with egg
sacs as described in experiment 1 and removed the egg sacs 24 h before
testing. Pardosa were fed crickets until sated 12 h before to
testing.
Stimulus preparation. Sixty Hogna were maintained in 12 cm diam x 8 cm high white plastic cups with clear lids (same containers used to house Pardosa in experiment 1). To standardize hunger levels, Hogna were sated with crickets, then fasted for 2 weeks before being used as experimental predators. We used two treatments for this experiment (n = 30/treatment): containers previously occupied by Hogna for 3 days and containers devoid of Hogna cues (control). Hogna helluo used as stimulus cues were fully satiated 24 h before introduction into the container, but were removed and replaced with a Hogna that had been sated then fasted for 2 weeks.
Measurement of Pardosa survival and statistics. After removal of the stimulus spider, but before adding the test Pardosa and predator, we increased heterogeneity by adding a small plastic vial wrapped in tape (4 cm long, 2.5 cm diam). Because the vial was added after the removal of the stimulus Hogna, it was devoid of predator silk or excreta. The vial was placed horizontally with its long axis close to the wall. The tape served to provide traction for the spider to climb on if it chose to do so. The space formed between the vial and wall was large enough to be occupied by Pardosa, but not Hogna. The opening of the vial was of a size that the predator could enter only with some difficulty. We placed a single adult, mated female Pardosa in each container that had an egg sac removed 24 h before the beginning of the experiment. The spider was allowed to acclimate for 1 h, after which we noted the position of the spider as being in the vial, on top of the vial, between the vial and wall on the ground, elsewhere on the ground, or on the wall exposed. Because spiders were only observed on the wall, on top of the vial, or elsewhere on the ground, we collapsed categories to wall, vial (on top), and ground. A single Hogna was introduced into the container at noon. Each container was monitored continuously for a 1 h period, every 5 min for the second and third hour, and once every 30 min thereafter for a 24-h period. Observations were suspended at 2200 h, and the room lighting was turned off and resumed at 0800 h when lighting was again turned on the next day. To compare the effectiveness of various Pardosa positions in the container as possible predator deterrents, we recorded the positions of spiders killed within the first 5 min of the experiment.
To analyze the effectiveness of being in a vertical position in deterring predation, we compared differences in Pardosa predation latency across peat moss treatments based on both the position of Pardosa and the presence of Hogna cues. We compared differences in the median time of predation by Hogna for each treatment using a Kaplan-Meier failure time analysis (log-rank test). Differences in space use in the container were tested using a chi-square test.
Results
Pardosa milvina survived much longer in the presence of
Hogna chemotactile cues than in containers lacking such cues. Based
on a Kaplan-Meier failure-time analysis, there was a highly significant
difference in the median time to predation between Hogna and control
treatments (log-rank test, 2 = 26.96, df = 1; p
<.0001; Figure 2).
Pardosa survived a median of only 8.83 ± 1.96 min in the
container without substratum-borne cues from Hogna, but survived a
median of 9.34 ± 0.709 h when Hogna cues were present.
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Pardosa showed a significant difference in their initial positions
in the containers with or without predator chemotactile cues
(2 = 21.86, p <.0009;
Figure 3A). In containers
without Hogna cues, most spiders were found resting on the top of the
vial, with fewer on the ground, and the fewest number positioned vertically on
the wall (Figure 3A). In the
Hogna treatment, the majority of spiders were occupying the wall with
equal numbers on the ground or vial top
(Figure 3A). After the first 5
min of introducing the predator, there were significant differences in
survival of spiders based on their position within the container
(2 = 32.80, p <.0001, n = 23). All
Pardosa that were vertically oriented on the walls survived, whereas
only 4 out of 19 spiders on the vial and 6 out of 14 spiders on the ground
survived (Figure 3B).
Chemotactile cues from predators elicit climbing behavior, but vertical
positions in the container are not favored by Pardosa when predators
are not present (Figure 3A).
The vertical orientation of Pardosa did significantly reduce
predation by Hogna (Figure
3B).
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Hogna were found to engage in nocturnal foraging because they preyed on Pardosa in nearly complete darkness between 2200 and 0800 h (Figure 2). During this time, nine Pardosa were captured and eaten in the absence of a light source. This indicates that Hogna probably located Pardosa through vibratory, tactile, and/or chemical cues.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONREFERENCES |
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Fitness-related costs due to chemically induced antipredator behavior have been commonly found within aquatic systems (Chivers and Smith, 1998
), but
far fewer analogous studies have been conducted in terrestrial systems.
Further, although many shifts in behavior have been documented in the presence
of either an actual predator or indirect cues associated with a predator, few
studies document if such changes in behavior actually result in reduced
predation when the predator is present
(Persons et al., 2001;
Venzon et al., 2000). Here we
document the occurrence of behavioral changes by prey due to chemotactile cues
from predators in a terrestrial arthropod. We also document that although
there are significant fitness-related costs to this shift in space use, it is
also an extremely effective antipredator behavior against the Hogna
producing the cues.
Our results suggest that climbing behavior is both energetically costly and
reduces prey capture efficiency. Spiders in experiment 1 were fed before
initial introduction into each treatment and were measured before a second
feeding. Measurements indicate that Pardosa were losing weight more
quickly in containers that previously contained Hogna. The difference
in weight loss could be attributed to physiological costs borne by the stress
of being under constant perceived predation risk and therefore may be
independent of whether spiders were exhibiting climbing behavior. However, the
majority of spiders climbed the sides of the container in the Hogna
treatment, unlike their behavior in the other treatment, which suggests a
larger energetic cost associated with maintaining a position on the side of
the container rather than the ground. Minimally, results indicate that the
spider's preferred location is not on the side of the container. Wolf spiders
are generally ground dwellers (Lowrie,
1968), and, unlike other ground-dwelling spiders such as
gnaphosids, clubionids, and corinnids, wolf spiders lack scopular hairs on the
most distal portion of the leg. Scopular hairs aid in adhering to smooth
surfaces (Foelix, 1996). Even
lycosid species such as Rabidosa rabida that typically are found in
herbaceous vegetation seem to prefer horizontal or gently sloping surfaces on
plants (Rovner and Knost,
1974). Pardosa lack scopular hairs at the tips of their
tarsi and were observed to have some difficulty climbing the sides of the
plastic containers.
The energetic costs of climbing behavior are compounded by the fact that
the presence of predator cues either inhibits feeding behavior or reduces
capture success. The feeding experiment indicates that spiders not only kill
fewer prey, but also eat fewer prey when in the presence of chemotactile cues
from a predator than in the presence of conspecific cues. There are a number
of nonmutually exclusive reasons that Pardosa may exhibit reduced
fruit fly predation in the containers with Hogna cues. Spiders may
have had difficulty capturing prey because they were residing on the side of
the container and therefore used their legs for maintaining their position
rather than lunging at prey. Pardosa that do lunge at prey while on
the side of the container are probably more likely to drop to the ground,
which, as our data show, is a more dangerous place to be if a Hogna
is present. Pardosa may have shown a decrease in activity in the
container with Hogna cues. Previous studies indicate that
Pardosa reduce activity levels in the presence of Hogna
chemotactile cues and that such behavior has a survival benefit
(Persons et al., 2001).
Decreased movement would have a negative impact on prey capture.
Increased energetic costs and the decreased foraging efficiency that results from residing in the presence of Hogna cues may have both contributed to reduced reproductive output. Spiders in the presence of Hogna cues produced fewer (though not significantly fewer) egg sacs than spiders in either conspecific or control treatments. Pardosa produced significantly lighter egg sacs and fewer eggs when exposed to predator cues for 2 weeks. We found no evidence that predator cues affect the latency to produce an egg sac, suggesting that the presence of Hogna chemical cues is not likely to have a large impact on the phenology of Pardosa. However, the presence of large numbers of predators could have a significant impact on Pardosa populations even if actual predation seldom occurs.
Although the reproductive and foraging costs for climbing behavior are high, the survival benefit of climbing may also be high. Spiders that climbed the sides of the container had 100% survival compared to individuals on the ground (42%) or vial top (21%) (Figure 3B). Climbing behavior appeared to be mediated primarily, if not exclusively, by the presence of Hogna cues on the substrate. Although Pardosa could presumably detect Hogna in the container through tactile cues, visual cues, vibratory cues through the substratum, and/or possibly even airborne volatiles, these sensory channels combined were insufficient to elicit high levels of climbing behavior. This suggests that detection of substratum-borne predator cues by the prey is the primary means of predator detection and is extremely important for survival in a Hogna—Pardosa encounter.
It is likely that the field equivalent to climbing behavior may be either
avoidance of the substrate or moving into the nearest available patch of
vertical vegetation. Adult Pardosa will avoid substrates containing
Hogna silk and excreta (Persons
et al., 2001). However, we suggest that simple avoidance of the
substrates containing predator cues does not fully explain observed climbing
behavior. Pardosa did not climb on the vial top, which was both
devoid of cues and horizontally oriented when Hogna cues were present
on the peat moss. This indicates that Pardosa did not climb the walls
and assume a vertical orientation only to avoid direct contact with
Hogna cues, but rather that vertical orientation may deter prey
capture by Hogna. Under natural conditions, it is unknown if
Pardosa will exhibit climbing behavior on the nearest vegetation when
encountering Hogna silk or excreta. Previous studies show that
Pardosa may show other effective defensive behaviors in the presence
of Hogna as well such as avoidance and decreased activity
(Persons et al., 2001). During
our collection of Hogna and Pardosa, we did observe that
Pardosa could be found in large numbers in soybean plants and high in
vegetation on some occasions, and strictly found on the ground at other times.
The cause for this shift in space use is currently unknown, but this study
suggests that predator avoidance cannot be ruled out as an explanation.
Our results are important in understanding predator—prey dynamics
among these two species. This study confirms the results of other experiments
that suggest that chemotactile cues alone induce antipredator behavior, not
the predator itself (Persons et al.,
2001). Also, Pardosa are capable of fine discrimination
between predators that pose different levels of predation risk. Spiders show
graded levels of activity depending on the diet of the Hogna
(Persons et al., 2001)
producing the cues. In light of our finding that defensive behaviors incur
significant fitness costs, exhibition of graded responses to different levels
of perceived risk may be a means of mitigating these costs. Other studies
suggest that indirectly mediated predator—prey interactions are much
more common in ground-dwelling spiders than previously realized. Punzo
(1997) found that wolf spiders
Schizocosa avida showed increased avoidance of substrates previously
occupied by the scorpion Centruroides vittatus if they had been
previously attacked by the scorpion than if they had never encountered it.
Wolf spiders may use chemotactile cues to locate prey more efficiently as
well. Persons and Uetz (1996)
found that the wolf spider Schizocosa ocreata spends longer periods
of time on substrates previously occupied by house crickets compared to
controls. Punzo and Kukoyi (1996) found that the wolf spider Trochosa
parthensus and the oxyopid Oxyopes salticus spend longer periods
of time on substrates previously occupied by prey common to their natural
habitat compared to cues from novel prey. Persons and Rypstra
(2000) found that H.
helluo prefer substrates previously occupied by their most recent prey
and also show attraction to chemotactile cues from Pardosa when fed
Pardosa.
These results clearly show that chemotactile detection of predators is critical for spiders to perform effective defensive behavior and that both the costs and benefits of climbing behavior are high. Spiders tended to remain on the sides of the containers for the entire time that Hogna cues were present, even when the actual predator was absent. This suggests that Pardosa may tend to overestimate predation risk and weigh the benefits of climbing behavior more heavily than the reproductive and feeding costs incurred by it. Selection pressure for Pardosa to respond to indirect predator cues is likely to be high. Future field studies will be necessary to verify the adaptive significance of chemotactilely mediated shifts in space use.
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ACKNOWLEDGEMENTS |
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Thanks are extended to Sam Marshall for technical assistance on this article. We also thank Doug Meikle for the use of lab space for this study and M. Brueseke, E. Henley, and Dean Ferrera for their help in collecting and maintaining spiders in the lab. Special thanks to Jon Hlivko for data collection. This research was funded by National Science Foundation grant DEB 9527710 (to A.R. and S. Marshall), the Department of Zoology, Miami University Research Challenge Grant, and the Hamilton Campus of Miami University.
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