Behavioral Ecology Vol. 10 No. 4: 422-427
© 1999 International Society for Behavioral Ecology
Direct and indirect cues of predation risk influence behavior and reproduction of prey: a case for acarine interactions
Laboratory of Entomology, Wageningen Agricultural University, PO Box 8031, 6700 EH Wageningen, The Netherlands
Address correspondence to M. Dicke. E-mail: marcel.dicke{at}users.ento.wau.nl
Received 17 June 1998; revised 16 September 1998; accepted 22 December 1998.
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ABSTRACT |
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Little is known about the flow of chemical information from higher to lower levels within the animal food chain. However, this information may determine the behavior and distribution of many animals (e.g., that of potential prey) when exposed to direct and indirect cues of predation risk. We used herbivorous spider mites, Tetranychus urticae Koch (Tetranychidae) as a model to examine the foraging and oviposition decisions that prey make when exposed to these cues. We conducted laboratory tests to determine if the previous presence of predators (direct cues) on leaf discs or the presence of injured conspecifics (indirect cues) alters the distribution of adults and eggs of T. urticae. When given a choice, after 24 h, fewer adults and eggs were found on leaf discs that had previously contained specialist spider mite predators, Phytoseiulus persimilis Athias-Henriot (Phytoseiidae), than on discs unexposed to predators. Also, more T. urticae emigrated from predator-exposed discs than from unexposed discs or from those that had previously contained nonpredatory mites (Tyrophagus putrescentiae, Acaridae). Finally, fewer T. urticae foraged and laid eggs on predator-exposed discs or on those with artificially damaged conspecifics (eggs or dead adults) than on discs with intact conspecifics. Tetranychus urticae probably recognizes infochemicals (kairomones) from its predators or cues from injured spider mites and consequently avoids feeding or ovipositing in areas exposed to these cues. Recognition and avoidance of kairomones from specialist predators by this prey are likely to be hereditary, but avoidance of injured conspecifics may be an adaptation to avoid predators that are not inherently recognized. We discuss the behavioral and ecological implications of our findings.
Key words: arthropods, infochemicals, kairomone, mites, Phytoseiulus persimilis, predator, Tetranychus urticae.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The foraging behavior of animals is shaped by energetic costs and by the risk from natural enemies (Krebs and Davies, 1987
). However, for the fitness of an organism, the
failure to detect natural enemies is usually more detrimental than, say, the
failure to detect food (Lima and Dill,
1990). An animal under strong selective pressure by higher trophic
levels will benefit from early detection of its enemies and from consequent
avoidance of a potentially lethal confrontation.
Many prey species evolved chemical senses (e.g., olfaction, taste) for
detecting their predators. Cues of predator presence may be direct [e.g.,
chemicals (kairomones); Dicke and Sabelis,
1992] emitted by the predators (e.g.,
Jedrzejewski et al., 1993;
Kriesch and Dicke, 1997;
Nolte et al., 1994), or
indirect [e.g., information from disturbed/injured (alarm pheromones) or dead
conspecifics; Chivers et al.,
1996; Janssen,
1998; Janssen et al.,
1997; Pijanowska,
1997; Rittschof and Hazlett,
1997; Vadas et al.,
1994].
When exposed to cues from predators or from injured conspecifics, many
animals have been shown to display defensive or evasive behavior. For example,
Daphnia magna respond to cues from crushed conspecifics by migrating
down the water column and forming small aggregations, a behavior that was
shown to reduce predation by fish
(Pijanowska, 1997). Geckos
(Coleonyx brevis) exhibit a defensive tail display when exposed to
skin odors of snake predators (Dial and
Schwenk, 1996). Snowshoe hares (Lepus americanus) and
voles (Clethrionomys glareolus, Microtus agrestis) may avoid
predation by reducing their feeding and breeding activity when perceiving
predator infochemicals (Koskela and
Ylönen, 1995;
Sullivan and Crump, 1986;
Ylönen and
Ronkainen, 1994). In fact, this type of response prompted attempts
to use predator products to reduce feeding damage by various mammal pests
(Coulston et al., 1993;
Engelhart and Muller-Schwarze,
1995; Sullivan et al.,
1991; Woolhouse and Morgan,
1995; Zimmerling and
Zimmerling, 1996). Finally, fruit flies (Rhagoletis
basiola, Tephritidae) were observed to delay oviposition when exposed to
chemical information from their egg parasitoids
(Hoffmeister and Roitberg,
1997). The different responses of prey to predator infochemicals
may depend on the relative risk posed by a predator species
(Marko and Palmer, 1991;
Vadas et al., 1994),
familiarity of prey with the chemical
(Chivers and Smith, 1994;
Dickman, 1992;
Mathis et al., 1996), and the
predator avoidance strategy of the prey
(Lima and Dill, 1990;
Malmqvist, 1992;
Vadas et al., 1994).
In this study, we used two-spotted spider mites, Tetranychus
urticae Koch and predatory mites, Phytoseiulus persimilis
Athias-Henriot, as a model system to observe the foraging and oviposition of a
herbivore when exposed to information about the potential risk of predation.
Tetranychus urticae are small, polyphagous mites (approximately 0.8
mm long; Sabelis, 1981) that
commonly infest commercial crops worldwide. They feed on the contents of leaf
cells and lay up to 20 eggs per day throughout their foraging area
(Sabelis, 1981;
Tomczyk and Kropczynska,
1985). Specialist phytoseiid predators, such as P.
persimilis, are the most effective natural enemies of T. urticae
(Sabelis, 1985).
Phytoseiulus persimilis feed on all stages of the spider mite by
piercing their prey with their mouthparts, and are capable of exterminating
entire populations of spider mites
(Sabelis and van der Meer,
1986).
We used the predators and the herbivores to test four hypotheses: (1) previous exposure of leaves to predators reduces oviposition by the spider mites, (2) when given a choice, T. urticae avoids foraging or ovipositing on leaves previously exposed to predators, (3) more spider mites emigrate from leaves exposed to predators than from leaves exposed to nonpredatory mites or from unexposed leaves, and (4) the spider mites avoid foraging and ovipositing on leaves that contain artificially damaged conspecifics.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Plants and mites
All experiments were conducted in a laboratory at 22°±2°C. For each experiment, we used discs (1 cm diam) cut from young, fully expanded leaves of lima bean (Phaseolus lunatus L.). Tetranychus urticae were reared on lima bean leaves and P. persimilis were reared on leaves that were infested by the spider mites. The mite colonies were maintained in a greenhouse (20°-30°C, 50-80% relative humidity). During experiments, we handled all mites and their eggs with fine brushes, using separate brushes for different mite species. For each trial, all open petri dishes or containers that housed the mites were placed in deep plastic trays, which were then covered with large sheets of paper to minimize air currents.
Reactions of T. urticae to previous predator presence
Exposure of leaf discs to predators
We used leaf discs that were either previously exposed to predators or
unexposed (clean). To obtain exposed discs, we introduced six adult female
P. persimilis and left the mites for 24 h
(Kriesch and Dicke, 1997). To
prevent predators from escaping, we placed the discs on water and left them
floating in open petri dishes. Approximately 2 h before each experiment
commenced, all predators and their eggs (if any were laid) were removed from
the leaves. Unexposed discs were also floating on water for 24 h, but without
predators.
Oviposition
Predator-exposed and unexposed discs (n = 70) were placed
separately on moist cotton wool in open petri dishes (one disc per dish). The
moist substrate kept the leaf tissue fresh for the duration of the test and
prevented the spider mites from leaving the discs. We placed one randomly
selected adult female T. urticae on every disc. After 24 h, we
counted the number of eggs laid by the spider mites in both treatments.
Choice
In this experiment, spider mites were offered a choice between two discs:
one predator exposed and one unexposed (clean). Thus, each petri dish
(n = 32) contained a level sheet of moist cotton wool, on which we
placed two leaf discs connected by a flat, T-shaped bridge (2.5 cm wide;
Figure 1A). The bridges were
cut from a transparent acetate sheet. The position of the discs relative to
one another (left/right) was randomized in each petri dish. We then released
six adult female T. urticae at the base of the T-bridge (see
Figure 1A). After 24 h we
counted the number of spider mite adults and eggs on each disc.
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Migration
We tested if spider mites will leave their initial food source and search
for other leaves if the original source had been exposed to predators. We also
examined if the spider mites have a similar response to leaves exposed to
other, nonpredatory mites or to unexposed leaves.
We placed two leaf discs, connected by a straight acetate bridge (13 cm long, Figure 1B) on moist cotton wool sheeting in open plastic containers (10x17 cm). Three setups were used, each consisting of 35 replicates of the following disc pairs: (1) one predator exposed and one control (freshly cut, clean), (2) one fungivore exposed and one control, and (3) one unexposed and one control.
Both unexposed and control discs were clean (i.e., no initial contact with mites). However, unexposed discs had been floating on water for 24 h (as in previous experiments), but control discs were cut from fresh leaves < 3 h before the trial. Cutting fresh discs reduced preparation time and controlled for the effect of floating the cut tissue (unexposed discs) for 24 h. Fungivorous mites consisted of Tyrophagus putrescentiae (reared by Koppert Biological Systems B.V., Berkel-Rodenrijs, The Netherlands). To obtain fungivore-exposed discs, 10 adult Tyrophagus females were placed on each disc, but predator-exposed discs were treated as in the previous experiments (6 P. persimilis per disc). The leaf discs were then left floating on water for 24 h. Fungivores were initially released in higher numbers than the predators because they were more likely to escape from the discs; at the end of 24 h, an average of five predators and five fungivores were retained per disc.
We removed all predators, fungivores, and their eggs from exposed discs before introducing the spider mites. We then placed six adult female T. urticae on each predator-exposed (treatment 1), fungivore-exposed (treatment 2), and unexposed disc (treatment 3). No mites were placed on the control (freshly cut) discs. After 24 h we compared the distribution of mites and of their eggs on the treatment and control discs.
Reactions of T. urticae to damaged conspecifics
Damaged adults
Pairs of leaf discs, connected by a T-shaped bridge (as in
Figure 1A), were placed on wet
cotton wool in each petri dish. Three treatments were used, in each of which
spider mites were offered a choice between two discs: (1) one with pierced
adult spider mites and one without mites (control), (2) one with intact, dead
adults and one without mites (control), and (3) one with pierced and one with
intact, dead adults (control).
We used 40 replicates for each treatment. In treatments that included T. urticae (either pierced or intact), six adult females were immersed in liquid nitrogen and thawed before being haphazardly placed on each disc. The mites were killed by freezing to avoid interference with the experimental animals. After placing the dead mites on discs, we pierced the individuals in treatments 1 and 3 with a fine needle, partially spilling their hemolymph. Finally, six live T. urticae females were released at the base of the bridge (similarly to Figure 1A). After 24 h, we checked the distribution of the live mites and of their eggs in each treatment.
Damaged eggs
We used paired leaf discs connected by T-bridges on wet cotton wool, as in
the previous experiment. However, this time, the following disc pairs were
used: (1) one with pierced eggs of T. urticae and one without eggs
(control), (2) one with intact eggs and one without eggs (control), and (3)
one with pierced eggs and one with intact eggs (control).
Where included, 10 recently laid (not frozen) eggs were haphazardly placed on each leaf disc. We pierced the eggs in treatments 1 and 3 with a fine needle. Six live spider mites were then released on the base of the bridge and monitored as for the previous experiment. Each treatment had 40 replicates.
Statistical analysis
In the oviposition experiment, we used ANOVA to compare the mean number of
eggs per disc that T. urticae laid on predator-exposed and on
unexposed discs. In the migration trial, we calculated the proportion of mites
and of eggs (out of the total number on both discs) found on the control disc
[i.e., Eggscontrol/ (Eggscontrol +
Eggstreatment)] for each replicate. We then normalized the data by
transformation with arcsin square root and compared means for the three
treatments with ANOVA. For all choice experiments (reaction to predators, to
damaged adults and to damaged eggs), we calculated the proportion of spider
mites and their eggs found on the control discs. We then used a t
test within each treatment to determine if the proportions of mites and eggs
on control (out of the total number on both discs) significantly differed from
0.5. Data for all experiments were checked for normality prior to the
analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Reactions of T. urticae to previous predator presence
Oviposition
Exposure of leaf discs to predators did not have a significant effect on oviposition by T. urticae (ANOVA: F1,138 = 1.65; p =.202). After 24 h, the spider mites laid an average of 3.5 (± 0.2 SE) eggs per disc on predator-exposed discs and 4.0 (± 0.3 SE) eggs per disc on unexposed discs.
Choice
When released on a T-bridge that connected predator-exposed and unexposed
leaf discs, the distribution of the spider mites and their eggs significantly
differed from a random (50: 50) distribution: 72 ± 6% of the adults
(t = 4.07, p =.0001) and 63±6% of their eggs
(t = 2.26, p =.028) were found on unexposed leaf discs after
24 h (Figure 2).
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Migration
When T. urticae were released on predator-exposed discs, after 24
h we found most of the mites and their eggs on the control, clean discs, 13 cm
away (Figure 3). However, when
the spider mites were released on fungivore-exposed and unexposed discs, more
mites and more eggs were found on the treatment discs than on the control
(Figure 3). The proportions of
adult T. urticae and of their eggs found on control discs showed an
overall difference among the three treatments (ANOVA, adults:
F2,100 = 7.37, p =.001; eggs:
F2,100 = 9.51, p <.001), although mite
distribution on fungivore-exposed and clean discs did not clearly differ
(Figure 3). Two replicates in
the fungivore treatment were accidentally disturbed during the experiment and
thus were excluded from the analysis.
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Reactions of T. urticae to damaged conspecifics
Damaged adults
When T. urticae were offered a choice between discs with pierced
conspecifics and clean discs (control), most adults foraged (t =
7.52, p <.001) and most eggs were laid (t = 9.59,
p <.001) on the control (Figure
4). Similarly, more spider mites (t = 3.88, p
<.001) and their eggs (t = 3.19, p =.002) were found on
clean leaf discs (control) than on discs that contained intact conspecifics
(Figure 4). However, when
offered discs with pierced versus those with intact (but dead) conspecifics,
most adults (t = 3.04, p =.003) and most eggs (t =
2.17, p =.033) were found on the disc with intact mites (control;
Figure 4).
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Damaged eggs
When we offered T. urticae a choice between clean discs and those
with pierced eggs, more eggs were laid on clean discs (t = 2.56,
p =.012), but the preference of adults for clean discs was marginally
insignificant (t = 1.69, p =.094;
Figure 5). There was no clear
preference in foraging (t = - 0.80, p =.425) or oviposition
(t = 0.99, p =.323) when mites were put on bridges that
connected clean discs and those with intact eggs
(Figure 5). Nevertheless, we
found more adults (t = 3.66, p <.001) and more eggs
(t = 3.10, p =.003) on discs with intact eggs than on those
with pierced eggs (Figure
5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The fitness of potential prey is favored when the prey forage and reproduce in areas that offer a minimal risk of predation. Chemical detection may be an important mechanism of risk assessment by prey (Tollrian and Harvell, 1999
),
but little is known about the ecological and evolutionary consequences of this
phenomenon. Our experiments show that, when given a choice, T.
urticae avoids foraging and ovipositing on leaves that had been
previously exposed to predators. Interestingly, the spider mites also left a
potential food source and traveled a considerable distance (equivalent to
about 163 body lengths) in search of other food if the original source had
been exposed to P. persimilis. In contrast, without predator
exposure, most of the prey remained and oviposited on their initial feeding
arena. This distribution effect is consistent with studies of other prey
(e.g., Jedrzejewski and Jedrzejewska,
1990; Utne and Bacchi,
1997).
In our experiments, each replicate consisted of a group of six spider mites
that may have influenced each other's distribution. The effect of conspecifics
on the distribution of individuals has been little studied for spider mites
(but see Bernstein, 1984;
Pallini et al., 1997).
However, spider mite populations often reach high densities in the field, and
they can relocate in groups (Rabbinge,
1985). Consequently, our use of six individuals per replicate is
likely in the field scenario and is consistent with previous studies of
migration by group-living prey (e.g.,
Malmqvist, 1992;
Pallini et al., 1997;
Pijanowska, 1997).
Many species of prey react to kairomones contained in the feces or other
secretions of their predators
(Buchanan-Smith et al., 1993;
Coulston et al., 1993;
Dial and Schwenk, 1996), and
the spider mites are probably no exception
(Kriesch and Dicke, 1997).
Learning through previous exposure to chemical cues also may play a role in
the response of the herbivores (see
Takabayashi et al., 1994),
similar to behavior shown by vertebrate prey
(Chivers and Smith, 1994;
Brown and Smith, 1996,
Mathis et al., 1996).
The chemicals that affect T. urticae are probably nonvolatile
(Kriesch and Dicke, 1997), but
their origin or nature is still unknown. For example, the prey may recognize
and avoid protein-derived metabolites that are common among many predatory
animals (Nolte et al., 1994).
If so, the mites should also react to nonspecialist or allopatric predator
species. Alternatively, the spider mites could react exclusively to traces of
conspecific alarm pheromones carried by the predators and spread on the
exposed discs. However, this is unlikely, as infochemicals from predatory
mites that were fed on alternative (insect) prey also triggered an avoidance
reaction among T. urticae (Grostal and Dicke, in preparation).
A variety of animals can distinguish cues of their predators from those of
nonpredatory animals (Appelberg et al.,
1993; Buchanan-Smith et al.,
1993; Cooper, 1990;
Jedrzejewski et al., 1993;
Kelly and Cory, 1987;
Sullivan, 1986;
Ward et al., 1996). In our
experiments T. urticae did not avoid leaves exposed to fungivorous
mites. Perhaps the spider mites distinguish infochemicals of their predators
from those of other, harmless species. Alternatively, the spider mites could
avoid areas with a wide range of foreign chemicals, but the amount of
kairomones deposited by T. putrescentiae differs from that deposited
by equal numbers of P. persimilis. T. urticae have been shown to
avoid leaf discs on which predator exposure per unit area was three times
lower (five P. persimilis on 2-cm diam discs;
Kriesch and Dicke, 1997) than
in our experiments (six P. persimilis on 1-cm diam discs). The
response of the spider mites to infochemicals of mite species from a broader
range of feeding groups is currently being investigated (Grostal and Dicke, in
preparation).
Unfavorable habitat conditions may suppress the fecundity of some species
even after mating (Ohgushi,
1996; Plotkin et al.,
1997), but little is known about whether predation risk can have a
similar effect. Although T. urticae preferred to lay more eggs in
areas that were relatively safe from predators, their oviposition on single,
isolated discs was not suppressed by exposure to cues from P.
persimilis, at least over 24 h. However, if the avoidance of predators
incurs a significant energetic cost (e.g., searching for alternative sites or
reduced feeding) or stress to the prey, size of adults and their oviposition
may be reduced in the long term. Conversely, energetic and reproductive
demands may incur trade-offs in predator avoidance (e.g., more frequent mating
in spite of a correspondingly higher risk of predation)
(Brown and Smith, 1996;
Lima and Dill, 1990). These
trade-offs remain unknown for terrestrial arthropods and should be examined in
the future.
Some animals show defensive responses to indirect cues of predator risk
(i.e., to information from damaged or alarmed conspecifics)
(Chivers et al., 1996;
Janssen, 1998;
Janssen et al., 1997;
Pickett et al., 1992;
Pijanowska, 1997;
Rittschof and Hazlett, 1997;
Vadas et al., 1994). The
reaction to indirect indications of threat is probably an adaptation to avoid
nonspecialist predators, or ones that are not inherently recognized by the
prey (Chivers and Smith, 1994;
Engelhart and Muller-Schwarze,
1995; Mathis et al.,
1996). Also, injured conspecifics probably provide an earlier
warning about predation risk than do predator products (e.g. feces), which
could be deposited after the attack on prey. In our experiments, spider mites
avoided leaves with damaged conspecifics (both eggs and adults), consistent
with several studies of other animals
(Chivers et al., 1996;
Pijanowska, 1997;
Vadas et al., 1994).
Interestingly, we also observed T. urticae to prefer empty leaves to
those that contained dead (frozen) adults. We offer three hypotheses to
explain this behavior. First, the spider mites may recognize dead conspecifics
and consequently avoid feeding arenas that show high conspecific mortality.
Second, the mites may choose areas that are free of potential competitors,
(i.e., leaves without other spider mites)
(Dicke, 1986; but see
Pallini et al., 1997). Third,
the dead animals may constitute an obstacle to feeding, and live adults may
choose to forage on more exposed leaf surfaces.
Most animals have a range of specialist and nonspecialist predators. However, the specificity and intensity of prey response to different types of predator remains little studied. Our results suggest that animals as simple as mites can have direct (predator cues) and indirect (prey cues) means of assessing predation risk. Whether the combination of cues from predators with those from damaged conspecifics has a synergistic effect on mite defenses or whether these cues affect the mites at a community level remains to be shown.
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