Behavioral Ecology
doi:10.1093/beheco/arr085
Advance Access publication 10 June 2011
Original article
Contact with caterpillar hairs triggers
predator-specific defensive responses
Ignacio Castellanos,a Pedro Barbosa,b Iriana Zuria,a Toomas Tammaru,c and Mary C. Christmand
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, A.P. 69–1, C.P. 42001,
Pachuca, Hidalgo, México, bDepartment of Entomology, University of Maryland, College Park, MD 20742,
USA, cDepartment of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu 51014,
Estonia, and dDepartment of Statistics, Institute of Food and Agricultural Sciences, University of Florida,
Gainesville, FL 32611, USA
a
Organisms have evolved morphological and behavioral traits that reduce their susceptibility to predation. However, few studies
have considered how morphological structures work to provide informational inputs necessary for effective behavioral responses
to predation risk. In this study, we demonstrate that the hairs of Orgyia leucostigma (Lymantriidae) caterpillars not only function as
physical barriers that deter predators but also act to provide sensory inputs triggering behavior that reduces predation risk. In
particular, the way in which caterpillars respond when their hairs are touched is predator specific. Mechanical parameters of the
interaction determining the response were identified correlatively and confirmed manipulatively. Caterpillars predominantly
dropped in response to high hair bending velocities and predominantly walked away in response to low hair bending velocities.
These stimulus-specific responses appear to be adaptive as they led to increased survival. Our results demonstrate a functional
link between morphology and behavior. The ability to respond effectively only after the initiation of a predator attack should
reduce the costs associated with antipredator behaviors. Key words: behavior, costs, defense, host, Lepidoptera, morphology,
Orgyia leucostigma, predation risk, signals. [Behav Ecol 22:1020–1025 (2011)]
INTRODUCTION
nimals have evolved different ways to reduce mortality risks
when exposed to predation, including physiological,
morphological, and behavioral defenses (Endler 1986; Sih
1987; Lima and Dill 1990). Behavioral defenses that reduce
susceptibility to predation involve reducing activity levels,
fleeing, and hiding (Lima and Dill 1990; Lima 1998).
Morphological defenses include a range of structures such
as protective spines and armor (Edmunds 1974; Gross
1993). Different types of antipredator defenses often function
at different stages in the predation sequence: primarily, either
before or after detection of the prey by a predator (Endler
1986; Sih 1987; Lima and Dill 1990).
Studies on antipredator defenses have often focused on
either behavior or morphology taken separately, even if
antipredator adaptations may frequently be complex in their
nature (e.g., Dewitt et al. 1999; Mikolajewski and Johansson
2004; Lind and Cresswell 2005; Arendt 2009). Moreover, the
effectiveness of prey morphological defenses is rarely evaluated against different predators (Murphy et al. 2010), while
not all predators are equally deterred by direct morphological
defenses of the prey (Eisner and Eisner 2000; Sandre et al.
2007). In such cases, the interplay between behavioral and
morphological defenses is far from straightforward, and the
attention on the phenotype as a whole must therefore be the
most fruitful way to understand predator avoidance.
In arthropods, specialized structures such as hairs, spines,
and thick sclerotized cuticles are thought to primarily function
A
Address correspondence to I. Castellanos. E-mail: ignacioe@uaeh.
edu.mx.
Received 25 November 2010; revised 15 April 2011; accepted 2
May 2011.
The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
as physical barriers that dissuade both predators and
parasitoids from attacking or reduce prey handling-success
after capture (e.g., Dyer and Floyd 1993; Gerling et al. 1998;
Riessen and Young 2005; Lindstedt et al. 2008; Rezak et al.
2008; Flenner et al. 2009; Murphy et al. 2010). However,
because these structures, when associated with sensory neurons, often act as cuticular mechanoreceptors that sense stimuli from outside the organism (McIver 1975, Zacharuk and
Shields 1991; Barth and Dechant 2003; Casas and Dangles
2010), they may also serve to provide information that triggers
behaviors necessary to evade, escape, or confront predators.
We investigated the role of defensive hairs of Orgyia leucostigma
J.E. Smith (Lepidoptera: Lymantriidae) larvae as touch detectors
under predator attack. We tested the hypothesis that the physically defensive hairs also provide sensory input triggering behavior that reduces predation and examined the possibility that the
response is predator specific, or more accurately, if it is specific
to the type of stimulus produced by different predators. Accordingly, we 1) analyzed whether antipredator behaviors of larvae
occur in response to stimulating their hairs, 2) determined if
predators that produce different rates of hair displacement elicit
different behavioral responses, 3) manipulated the possible
antipredator behavioral responses of larvae to determine
whether the differential responses against different predators
may be adaptive, and 4) determined if hair removal reduces
the possibility that caterpillars escape from predation.
MATERIALS AND METHODS
Study organisms
Prey species
Larvae of the nearctic O. leucostigma are covered with
conspicuous defensive hairs (Figure 1), with some of the tufts
Castellanos et al.
•
Caterpillar hairs trigger defensive responses
Figure 1
An Orgyia leucostigma caterpillar. Photograph by D.L. Wagner, with
permission.
exceeding in length the diameter of the body (Payne 1917).
The polyphagous larvae are external solitary feeders on the
foliage of deciduous trees. Orgyia leucostigma larvae used in the
experiments originated from a laboratory colony established
from larvae collected from Acer negundo L. (Aceraceae) (box
elder) trees in Patuxent Wildlife Refuge Research Center, MD,
USA. Larvae eclosing from egg masses were reared individually in 237-ml plastic containers, being fed box elder foliage.
Predator species
The predators used in this study had been identified as common
members of the insect community in tree canopies in Patuxent
(Barbosa P, Castellanos I, Segarra AE, unpublished data). The 3
invertebrate predators of caterpillars included in the study were
the adults of the wasp Polistes fuscatus Fabricius (Vespidae), the
stink bug Podisus maculiventris Say (Pentatomidae), and the
spined assassin bug Sinea diadema Fabricius (Reduviidae). These
predators were chosen to represent different modes of action.
Adults of P. fuscatus capture and process caterpillars to feed
their larvae (Michener and Michener 1951; Rabb 1960; Gould
and Jeanne 1984; Raveret Richter 2000). Hunting Polistes
wasps appear to detect prey items from some distance when
hovering, either visually or chemically, and they pounce upon
they prey thereafter (Stamp 1992; Stamp and Wilkens 1993).
Podisus maculiventris is a generalist predator that feeds primarily on larval Lepidoptera and Coleoptera (McPherson 1982).
Stink bugs actively search for prey while walking on the foliage
of plants, responding to prey within a few millimeters or after
physically contacting the prey (Evans 1982). Upon encountering prey, P. maculiventris extend their beak and slowly attempt to
insert it into the nearest part of the prey (Evans 1982).
Sinea diadema is a generalist predator that attacks a diverse
range of arthropod species (Readio 1924). A foraging adult
typically employs a sit wait strategy for capturing prey with its
raptorial forelegs (Taylor and Schmidt 1996). It locates and
approaches prey items using antennal olfaction and extends
its raptorial forelegs that are used for grasping prey (Taylor
and Schmidt 1994; Freund and Olmstead 2000).
All predator individuals used to start laboratory colonies
were collected from the Patuxent Wildlife Refuge Research
Center. Colonies of all predator species were maintained in
the laboratory and were provided with larvae of various insects.
Experimental protocol
Behavioral responses to predator attacks
An individual trial consisted in exposing a larva of O. leucostigma to a predator in an experimental setting, in the labora-
1021
tory at room temperature. For each trial, we recorded the
behavioral responses of the larvae after predator contact with
protective hairs. Three types of responses were observed:
dropping off the leaf, walking away from the predator, or no
reaction at all. We also noted the predator body part (i.e.,
antennae, mouthpart, or leg) that came in contact with larvae
when a response was observed. Orgyia leucostigma larvae were
considered survivors when the predator left the experimental
leaf with the larva unharmed. The predators were starved
before the experiments to increase their motivation to attack
larvae.
A total of 23 trials were conducted with P. fuscatus, 21 with
adult P. maculiventris, and 20 with adult S. diadema. In each
trial, a third-instar O. leucostigma larva was placed on the leaf of
a 15-cm A. negundo branch positioned 0.5 m above the ground
and was allowed to acclimate for half an hour. The branch had
been placed inside a vial with water and fixed with a clamp to
a vibration-isolating table (Newport LW3048B-OPT). Different
predator and prey individuals were used for each behavioral
trial. In experiments, P. fuscatus wasps flew from their nest to
the experimental leaf, whereas P. maculiventris and S. diadema
individuals were placed on a vertical stem in contact with the
experimental leaf. All trials were conducted in the laboratory
at room temperature of about 25 6 2 C.
Caterpillar hair displacement by predators
To quantitatively characterize the interaction of the predators
with larval hairs, the encounters of the insects were videotaped.
Encounters between predators and caterpillars were filmed at
30 frames per second. Hair displacement velocities were calculated from replayed video sequences. This was facilitated by
a 1-mm2 grid having been placed behind the leaf on which
predators and prey interacted. Six attacks by wasps, and 9
attacks each by stink bugs, and spined assassin bugs were
analyzed.
Responses to controlled stimuli
Hair displacement was mechanically reproduced to mimic
velocities produced by the different predators. Hairs were bent
with a single sinusoidal wave of either 1.0 or 0.01 Hz. The 1-Hz
stimulus resulted in a velocity within the range produced by
both P. fuscatus and S. diadema during contact with hairs
(maximum hair tip velocity of 30 mm/s), and the 0.01-Hz
stimuli resulted in a velocity within the range produced by
P. maculiventris (maximum hair tip velocity of 0.75 mm/s).
Both stimuli were adjusted to have the same displacement.
The sinusoidal waves were produced with a waveform
generator (Agilent Technology, Santa Clara, CA/Hewlett
Packard 33120A), amplified with a power amplifier (Labworks
PA-119) and connected to an electrodynamic shaker (Labworks ET-132-2). Contact with larval hairs was achieved using
an excised antenna of a P. fuscatus wasp that was glued to
a base attached to, and extending 7 cm from, the armature
of the shaker. The mechanical displacement was longitudinal
with respect to the caterpillar in order to bend dorsal hairs
perpendicularly to their base because most of the attacks by
the predators had been observed to occur along this axis. Hair
displacement was applied approximately 1 mm from the base
of dorsal hairs, and the stimuli were not strong enough to
mechanically knock down larvae. We exposed 42 caterpillars
to the 1-Hz stimulus and 33 caterpillars to the 0.01-Hz stimulus. The setup of the experiment was identical to that used
with the real predators.
Consequences of responses to predators
Once we had determined the differences in behavioral
responses of larvae to each predator, we also recorded the consequences of the responses to larval survival by manipulatively
Behavioral Ecology
1022
restricting the set of possible reactions. Third-instar O. leucostigma were 1) allowed to respond by dropping or walking
(larvae were placed on a leaf of a 15-cm box elder branch
positioned 0.5 m above the ground), 2) the larvae were able
to walk but not drop (larvae were placed on a box elder leaf
on the ground), or 3) the larvae were unable to either drop or
walk (larvae were tied to a leaflet of a 15-cm box elder branch
positioned 0.5 m above the ground). Larvae were then exposed to individual foraging wasps, stink bugs, or spined assassin bugs. A caterpillar was recorded as a survivor when the
predator or the larva left the leaf with the larva remaining
unharmed.
Sample sizes for larvae allowed to respond by dropping or
walking were 23 for P. fuscatus, 20 for S. diadema, and 21 for
P. maculiventris; for larvae allowed to respond by walking or
not allowed to respond by dropping or walking, the sample
size was 16 for each predator. All trials were conducted in the
laboratory at an ambient temperature of about 25 6 2 C
Hair removal and caterpillar survival
The hairs of 45 third-instar O. leucostigma larvae were cut with
curved dissecting scissors, leaving hair shafts approximately
0.5 mm long (the hair removal treatment, hereafter). Of these
45 caterpillars, 15 were exposed to each of the 3 predators
(wasps, spined assassin bugs, and stink bugs). In order to
control for the possible effect of the procedure of hair cutting
per se, we only cut approximately 0.5 mm of the tips of the
hairs of 60 third instars (providing a clipping control). Of
these 60 control caterpillars, 20 were exposed to each of the
3 predators and their survival was compared with that of caterpillars subjected to the hair removal treatment. A caterpillar
was recorded as a survivor after the predator or the larva left
the leaf.
Statistical analyses
The frequencies of different behavioral responses of caterpillars and of the consequences of the responses to predators, as
well as differences in survival, were compared among treatments using chi-square tests of independence or Fisher’s exact
tests when the assumptions of the chi-square test were not met
(Agresti 1996). Hair bending velocities prior to the initiation
of an antipredator behavior were compared using a nonparametric Kruskal–Wallis analysis of variance. The family-wise
error rate for multiple comparisons was controlled using a
Bonferroni correction (Sokal and Rohlf 1995). We report
means 6 standard error.
RESULTS
Behavioral responses to predator attacks
The behavioral responses of O. leucostigma larvae to the different predators invariably occurred as soon as their hairs were
touched; contact with the body was not necessary. The caterpillars that escaped from wasps (13 out of 23) did so in response to touch by a wasp’s antennae (62% of survivors),
mouthpart (23%), or leg (15%). Caterpillars that escaped
from stink bugs (16 out of 21) did so in response to touch
by the beak (93% of survivors) or the stink bug’s antennae
(7%). All the caterpillars that escaped from spined assassin
bugs (15 out of 20) did so in response to touch by an assassin
bug’s foreleg.
The array of behaviors displayed by caterpillars (i.e., dropping, walking, or lack of a response) in response to predator
contact with their hairs depended on the predator making the
contact (Figure 2). All the caterpillars that escaped predation
from wasps and spined assassin bugs did so by dropping from
Figure 2
The behavioral responses of Orgyia leucostigma caterpillars that survived
from the attacks of Polistes fuscatus (wasps) (N ¼ 13), Sinea diadema
(spined assassin bugs) (N ¼ 16), and Podisus maculiventris (stink bugs)
(N ¼ 15). All the behavioral responses occurred as soon as the defensive
hairs were touched by predators. The type of behavioral responses of
caterpillars depended on the predator to which they were exposed
(Fisher’s Exact test P , 0.0001). Walk ¼ caterpillars that escaped by
walking away from the predator, Drop ¼ caterpillars that escaped by
dropping from the leaf, No response ¼ caterpillars that did not
respond to predators and were not eaten.
the leaf, whereas the response to stink bugs was more diverse
(Figure 2). The percentage of caterpillars that dropped in
response to stink bugs (26.6%) was significantly smaller than
the percentage of caterpillars that dropped in response to
wasps and spined assassin bugs (Fisher’s Exact test: P ,
0.0001).
Caterpillar hair displacement by predators
The displacement velocities of hairs differed among predators
(v2 ¼ 16.59, degree of freedom [df] ¼ 2, P ¼ 0.0003). The
velocities at which wasps, spined assassin bugs, and stink bugs
bent hairs were 86 mm/s 6 18 (N ¼ 6), 152 mm/s 6 34 (N ¼
9), and 0.40 mm/s 60.13 (N ¼ 9), respectively. Hair displacement velocities did not differ between wasps and spined assassin bugs (v2 ¼ 0.78, df ¼ 1, P ¼ 0.4). Wasps, which pounce on
their prey, and spined assassin bugs, which strike at their prey,
elicited O. leucostigma dropping behaviors, and both species
bent hairs with significantly higher velocities than stink bugs
(v2 ¼ 10.29, df ¼ 1, P ¼ 0.004, and v2 ¼ 12.90, df ¼ 1,
P ¼ 0.009, respectively, with Bonferroni correction).
Responses to controlled stimuli
Mechanically simulated predator attacks confirmed that the
behavioral responses of O. leucostigma caterpillars depended
on the rate at which the hairs were bent (v2 ¼ 34.65, df ¼ 2,
P ¼ 0.001). Larvae predominantly dropped (66.7%) in response
to the 1-Hz stimuli (reproducing the hair bending velocity of
wasps and spined assassin bugs) (v2 ¼ 22.48, df ¼ 1, P ¼ 0.001)
and predominantly walked (78.8%) in response to the 0.01-Hz
stimuli (hair bending velocity of stink bugs) (v2 ¼ 34.09, df ¼ 1,
P ¼ 0.001) (Figure 3).
Consequences of responses to predators
Survival among manipulated caterpillars differed significantly
among treatments (i.e., able to drop, able to walk, or deprived
Castellanos et al.
•
Caterpillar hairs trigger defensive responses
Figure 3
The behavioral responses of Orgyia leucostigma caterpillars to 2
mechanically produced bending velocities of their hairs. The 1-Hz
velocity represented the hair displacement velocity produced by the
predators Polistes fuscatus and Sinea diadema, and the 0.01 Hz
represented the hair displacement velocity produced by Podisus
maculiventris. Both stimuli were adjusted to have the same
displacement of 1.2 cm. **P , 0.01.
from the possibility to respond) when the larvae were exposed
to wasps (Fisher’s Exact test: P , 0.0001), stink bugs (v2 ¼
13.56, df ¼ 2, P ¼ 0.001), and spined assassin bugs (v2 ¼
9.34, df ¼ 2, P ¼ 0.009). When exposed to foraging wasps,
the survival of caterpillars that were allowed to drop (the
behavior representing the response to wasps and spined assassin bugs; Figure 4) was significantly higher than the survival of
caterpillars that were allowed to walk only (the behavior representing the response to stink bugs; Figure 4) or caterpillars
that were prevented from both dropping or walking (representing no response; Figure 4) (v2 ¼ 13.56, df ¼ 1, P ¼ 0.002,
and v2 ¼ 13.56, df ¼ 1, P ¼ 0.002, respectively). When exposed to stink bugs, no difference in survival was found between caterpillars that were allowed to drop or only walk (v2 ¼
0.02, df ¼ 1, P ¼ 0.893) and both resulted in significantly
higher survival than nonresponding caterpillars (v2 ¼ 10.86,
1023
Figure 5
Survival of Orgyia leucostigma caterpillars with hairs (clipping control)
and removed hairs to the attacks of Polistes fuscatus (wasps), Sinea
diadema (spined assassin bugs), and Podisus maculiventris (stink bugs).
*P , 0.05, **P , 0.01.
df ¼ 1, P ¼ 0.002, and v2 ¼ 10.49, df ¼ 1, P ¼ 0.002,
respectively) (Figure 4). When exposed to spined assassin
bugs, the survival of caterpillars that were allowed to drop
did not differ significantly from the survival of caterpillars that
were allowed to walk (Fisher’s Exact test: P ¼ 1) and both
resulted in significantly higher survival than nonresponding
caterpillars (v2 ¼ 6.76, df ¼ 1, P ¼ 0.036, and v2 ¼ 6.35, df ¼ 1,
P ¼ 0.036, respectively).
Hair removal and caterpillar survival
Survival was more than 2 times greater for caterpillars with
hairs than for caterpillars without hairs for the 3 predators.
Caterpillar survival was significantly reduced when attacked by
wasps, spined assassin bugs, and stink bugs (v2 ¼ 5.60, df ¼ 1,
P ¼ 0.018, v2 ¼ 16.13, df ¼ 1, P ¼ 0.001, and v2 ¼ 4.64, df ¼ 1,
P ¼ 0.031, respectively) (Figure 5). The survival for the no-hair
caterpillars did not differ among predator types (Fisher’s Exact
test: P ¼ 0.245, N ¼ 15).
DISCUSSION
Figure 4
The survival of larvae of Orgyia leucostigma that were able to drop (the
behavior representing the response to wasps and spined assassin
bugs), walk (the behavior representing the response to stink bugs),
or deprived from the possibility to respond, when exposed to Polistes
fuscatus (wasps), Sinea diadema (spined assassin bugs), and Podisus
maculiventris (stink bugs). *P , 0.05, **P , 0.01.
Most predator–prey studies that have investigated antipredator defenses have focused on either behavior or morphology,
giving little consideration to the interplay between these 2
functional characteristics. This study shows that in a lepidopteran larva, morphology and behavior are linked and act complementarily in an adaptive way when its antipredator defense
is built up.
Larval hairs were shown not only to provide a signal about
the incidence of predator attack but they also transmitted information about the type of predator. In particular, the differences in behavioral responses by larval O. leucostigma were
based on differences in the velocity at which their hairs were
bent. During attacks on larval prey, both wasps and spined
assassin bugs generated high hair displacement velocities that
triggered a dropping behavior. In contrast, stink bugs, which
generated low displacement velocities, triggered mainly a walking response. Similarly, caterpillars predominantly dropped in
response to mechanically reproduced high hair bending velocities and predominantly walked away in response to
mechanically reproduced low hair bending velocities.
The specificity in the responses of caterpillars to stink bugs
and wasps appears to be adaptive in the light of the results of
Behavioral Ecology
1024
the present study. When attacked by P. maculiventris, caterpillars predominantly responded by walking away. This was an
adequate response because survival increased compared with
that of caterpillars that were deprived from the possibility of
responding. On the other hand, results of the experiments
with P. fuscatus showed that survival of larvae increased only if
they could drop. This difference in the behavioral response of
O. leucostigma to stink bugs and wasps may be determined by
the cost associated with dropping. Dislodged larvae will require reaching another host tree and could be subjected to
ground predation (Losey and Denno 1998; Nelson 2007; Castellanos I, Barbosa P, Caldas A, unpublished data).
Nevertheless, larvae of O. leucostigma dropped in response to
spined assassin bugs even if walking away was shown to be
sufficient to escape from this predator. Two possible explanations may account for the seemingly maladaptive dropping
behavior by O. leucostigma in response to assassin bugs. It is
well likely that this species of prey has not evolved a sensory
system that allows it to distinguish among the signals produced by wasps and spined assassin bugs, both of which produce high hair displacement velocities. Alternatively, larvae
may still be able to detect differences among the signals (assassin bugs generated higher displacement velocities than
wasps), but the signal produced by S. diadema may be within
the range produced by other fast hair displacement predators
that can predate on caterpillars that escape by walking (see
Djemai et al. 2001; Caldwell et al. 2009).
Air currents generated by the wing beats of approaching
predators (Tautz and Markl 1978; Triblehorn and Yager
2006) and substrate borne vibrations produced by invertebrate predators walking on a leaf (Castellanos and Barbosa
2006) can alone cause insects to respond defensively. However, these stimuli are unlikely to account for the behaviors
of O. leucostigma observed in this study. First, larvae invariably
showed defensive behaviors only after their hairs were
touched and displaced, either by predators or controlled stimuli. Indeed, tactile hairs are not displaced by airflow, they are
deflected by much larger forces resulting from direct contact
with a stimulating object (Barth and Dechant 2003). Second,
spined assassin bugs and stink bugs forage for prey by walking
and stop for several seconds (sometimes minutes) near larvae
before making contact with their hairs, and most of the attacks
by wasps occurred while the predators were walking, after
having landed on leaves (Castellanos I, personal observation).
The behavioral responses of O. leucostigma caterpillars (no
reaction, walking, and dropping) represent increasingly
strong responses. Such graded reactions have previously been
attributed to different stimulus intensities produced by predators that approach insect prey from a distance (Markl and
Tautz 1975; Fullard 1979; Yager et al. 1990; Schulze and Schul
2001; Jones et al. 2002; ter Hofstede and Fullard 2008), and
the results of this study actually conform to this qualitative
pattern, however, our study is novel because it also provides
a quantitative analysis of this pattern. Nevertheless, our design
did not allow us to separate the different parameters of the
signal: a stimulus causing a higher hair bending velocity was
necessarily also more intense. An exciting area for further
studies would be to diversify the artificial stimuli in order to
determine the number of parameters of a signal a prey animal
is able to distinguish.
This study shows that the hairs of larvae of O. leucostigma
provide at least 2 advantages in the presence of invertebrate
predators: in addition to providing the sensory input needed
to trigger predator-specific behavioral responses, they physically hamper predator strikes. The latter aspect is illustrated
by the tendency of the larvae with their hairs removed to be
more vulnerable to predators. At the present, however, we do
not know if the same (e.g., Markl and Tautz 1975) or different
types of hairs (e.g., Paydar et al. 1999; Hiraguchi et al. 2003)
are responsible for the predator-specific responses.
Most studies on behavioral responses of prey to predator stimuli have been conducted on prey individuals that respond before
they are attacked or captured, that is, from a distance (Hoy et al.
1989; Lima and Dill 1990; Curio 1993; Kats and Dill 1998; Dicke
and Grostal 2001). In this study, we have demonstrated that
caterpillars also are able to respond differentially to stimuli produced by predators even during contact, that is, after an attack
has initiated, and that the response appears adaptive. Responding effectively only after a predator has initiated an attack offers
an opportunity to reduce the costs associated with antipredator
behaviors (Abrams 1994; Bouskila et al. 1995). This may be
a useful strategy given that even though predators may be in
proximity to prey they may not always attack or capture a prey.
Although hairs may represent a substantial initial energetic
investment (Bowers 1993; Montlor and Bernays 1993), they
may be relatively inexpensive to maintain. Furthermore, they
also may be involved in other essential functions such as thermoregulation (Casey and Hegel 1981; Kukal et al. 1988) and
crypsis (Sandre et al. 2007). More research is needed that
integrates both morphological and behavioral antipredator
defenses, particularly the functional link between antipredator morphology and behavior, their relative costs, and the
consideration of multiple functions in the evolutionary
‘choice’ of an anti-predator defense.
FUNDING
FOMIX Hidalgo segunda fase (grant number 95828 to I.C.);
Estonian Science Foundation (grant 7522, targeted financing
project SF0180122s08 to T.T.); European Union through the
European Regional Development Fund (Center of Excellence
FIBIR).
We acknowledge the able assistance of Holliday Obrecht of the
Patuxent Wildlife Research Center for his invaluable support of this
research. We acknowledge the immensely helpful suggestions provided
by D.G. Bottrell, R.F. Denno, and D.D. Yager. I.C. thanks the Universidad Autónoma del Estado de Hidalgo, México, the Programa de Mejoramiento del Profesorado (PROMEP), Secretarı́a de Educación Pública,
México, and FOMIX Hidalgo 95828, segunda fase for their generous
support. T.T. was supported by the Estonian Science Foundation grant
7522, targeted financing project SF0180122s08 and by the European
Union through the European Regional Development Fund (Center
of Excellence FIBIR).
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