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First published online August 31, 2007
Journal of Experimental Biology 210, 3165-3170 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.004648
Escape performance decreases during ontogeny in wild crickets
1 Université de Tours, IRBI UMR CNRS 6035, Parc Grandmont, 37200
Tours, France
2 IRD (R072), c/o CNRS LEGS, BP1, 91198 Gif-sur-Yvette cedex,
France
* Author for correspondence (e-mail: dangles{at}legs.cnrs-gif.fr)
Accepted 11 June 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: ontogeny, field experiment, crickets, antipredator behaviour, cercal system
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Irschick,
2003; Vanhooydonck and Van Damme, 2003;
Irschick et al., 2005).
Factors related to the performance of organisms operate within an ecological
context and are subject to complex interactions with other intrinsic (e.g.
age, experience, learning) and extrinsic variables (e.g. predator type,
habitat characteristics). Among them ontogeny is a major factor that can
influence the level of ecological performance within natural populations as it
affects a broad range of ecological, physiological and behavioural
characteristics (see Roth and Johnson,
2004). However, studies investigating changes in the performance
of animal function with ontogeny are restricted to relatively few groups of
organisms, mainly vertebrates, and few traits, such as locomotor and feeding
systems. Little consideration is generally given to the ecological context in
which these traits take place and are selected
(Irschick, 2003;
Herrel and Gibb, 2006). Of
particular ecological and evolutionary relevance are traits related to escape
performance, as they are directly related to the survival and, therefore, the
fitness of organisms (O'Steen et al.,
2002; Walker et al.,
2005). Most studies have focused on the kinematics of various
locomotor behaviours displayed during escape, for example sprinting and
jumping (Thompson and Kier,
2002). However, from an evolutionary perspective, organisms are
likely to adapt to predation risks at an earlier detection stage of the
predation sequence, as it confers substantial selective advantages for prey
(Endler, 1991;
Fox et al., 2001).
Arthropods (e.g. insects and spiders) are good models of evolved high
performance detection systems; they have hundreds of mechanoreceptive
cuticular hairs, which are sensitive to touch (filiform hairs) or wind
currents (trichoid hairs) generated by approaching predators
(Tautz and Markl, 1978;
Gnatzy, 1996;
Suter, 2003). The sensing
performance of animals greatly influences their ability to detect and escape
predators. Prey with high performance levels of detection may achieve greater
fitness levels in nature, up to a certain point. Given that juveniles
generally suffer higher rates of predation than adults, selection for
mechanisms that improve juvenile escape performance is likely to be strong.
This is observed in wood crickets (Nemobius sylvestris Bosc), a
widespread detritivorous insect, foraging on leaf litter of deciduous European
forests. Wood crickets suffer high rates of predation by wolf spiders
(Pardosa sp.), especially during juvenile instars
(Dangles et al., 2006a).
Crickets have evolved one of the highest performance anti-predatory sensory
systems (Shimozawa et al.,
2003) and because the structure of their mechano-sensory system
varies throughout development (Dangles et
al., 2006c), we expect there to be strong selective forces acting
on their escape performance during ontogeny.
The relationship between performance and body size of organisms remains
controversial. Many studies have reported that as animals get larger
performance levels increase or remain constant
(Irschick, 2000;
Trillmich et al., 2003).
Recently, there have been reports describing a decrease in performance
throughout ontogeny (Gibb et al.,
2006). Previous research on performance remains dominated by
studies relating to vertebrates and nothing is known about the ontogenic
changes relating to invertebrate performance. We measured ontogenic changes
and their effects on performance (measured as the escape distance) in wild
wood crickets behaving freely under natural conditions. We devised a portable
actuator that mimicked the attack dynamics of natural predators on crickets,
for example wolf spiders. We quantified the cricket escape performance and
behaviour by analysing numeric film sequences obtained with a high-speed video
camera.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Mean
cercus lengths were varied: 1.1 mm in juveniles I, 1.9 mm in Juveniles II, and
4.5 mm in adults. Only young adults displaying a high level of foraging
activity were selected to exclude senescent individuals. All crickets were
collected from an oak forest in the vicinity of Tours, France
(47°17'06''N, 00°47'13''E) the day before the
experiment. The crickets were housed in plastic boxes filled with layer of
leaves after capture, fed with dry cat food, and watered using wet cotton
swabs.
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). The
acceleration and velocity of the piston displacement was driven easily and
with high precision (±4%) using specific macro commands via
hyperterminal software and the rs232 port of a laptop
(Fig. 1A; B). This allowed us
to control and set it to mimic a spider attack. We had previously validated
this device using particle image velocimetry (PIV) analyses of the air-flow in
front of the moving piston (see Dangles et
al., 2006b). The piston displacement produces a flow pattern very
similar to that produced in front of a running spider. Initially, the piston
was fixed to an actuator, which could not be easily moved under field
conditions to follow wandering crickets. Therefore, we added a 1.5 m wire
between the actuator and the tip of the piston to facilitate its use
(Fig. 1A; A,C). Cricket escape behaviour was recorded using a lightning RDT1 high-speed (HS) digital video camera (Fig. 1A; D) (DRS Data & Imaging Systems, Inc., Oakland, NJ, USA) with a frame rate of 1000 frames s–1 and resolution of 1280x512 pixels. The escape response for freely behaving animals was recorded by following a cricket with the camera after its initial release until it stopped moving. The camera was mounted on a ramp (Fig. 1A; E) fixed on the rotating head of a stable tripod 0.5 m above the ground (Fig. 1A; F). This system allowed us to follow cricket displacements within a 2.5 m diameter. The size of the image on the camera was only about twice the size of the cricket, providing sufficient detail for measuring escape distances, but making it difficult to keep the moving cricket centred on the camera screen. We overcame this problem by fixing a red laser pointer (Fig. 1A; G) to the camera support in such a manner that pointing the laser on the cricket body ensured that the cricket was well-centred on the camera. The ground was illuminated by a halogen lamp (Fig. 1A; H) located 1 m above the ground surface. The video acquisition was controlled using a laptop (Fig. 1A; I) equipped with a DA170M data acquisition board (4 Gb of memory) and MIDAS 2.0 software (Xcitex Inc, Cambridge, USA).
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)]. Once the
cricket was motionless, the piston was placed rear-on 4.5 cm from the cricket:
this is the median distance at which spiders attack wood crickets
(Dangles et al., 2006b). The
piston was positioned at the height of a spider, 0.2 cm above ground. The
piston was launched at an attack angle of ±20° from the rear of the
cricket, to make sure that crickets relied only on their cercal system for
detection. The piston travelled far enough to touch the cricket. The cricket
escape behaviour was recorded by the HS camera
(Fig. 2).
The kinematics of the spider run is composed of a short initial
acceleration over 1 cm followed by a phase of relatively constant velocity up
to prey (Dangles et al.,
2006b). Piston kinematic was set up to mimic these properties.
Moreover, we simulated various piston velocities because wolf spiders modulate
their attack velocity when preying on crickets (see
Dangles et al., 2006b), thus
increasing the ecological relevance of our biological test. We chose three
attack velocities within the range of those recorded for spider attacks (see
Dangles et al., 2006b): slow
(40 mm s–1), intermediate (150 mm s–1) and
fast (300 mm s–1) attack. In total, 90 individuals (10
replicates x 3 instars x 3 velocities) were tested in a randomised
set-up to avoid any of them adapting to the piston velocity.
Behavioural measurements
Crickets regularly respond to a wind stimulus by first turning their bodies
consistently away from the danger source (by e.g. 60–90°) with a
short latency and then by walking/running or jumping
(Stabel et al., 1985;
Tauber and Camhi, 1995).
Pivoting is time-consuming, but this strategy appears to be adaptive in
escaping from natural predators [as suggested for cockroaches
(Camhi et al., 1978)]. In the
present study, we determined two variables for each HS video recording: (1)
the type of escape (walking or jumping) and (2) the escape angle, i.e. the
body angle of the cricket at the moment of escape relative to the direction of
the piston.
Performance measurements
The escape performance by evading crickets was expressed as a function of
their escape distance, i.e. the distance between the cricket and the piston at
the time the cricket initiates its escape. The escape performance was divided
into two categories, depending on whether the cricket escaped before or after
being touched by the piston. (1) The escape distance before contact between
the cricket and the piston; this was the straight-line distance between the
tip of the cercus and the tip of the piston in the frame prior to cricket-leg
flexion, either to turn (most cases) or directly jump/walk (few cases). This
measured the air-evoked escape performance of the cricket. (2) The escape
distance after contact between the piston and the cricket; this was the
distance between the location of the tip of the piston in the frame of contact
and its location in the frame prior to cricket-leg flexion. This is an inverse
measurement for touch-evoked escape performances in crickets. Therefore, an
escape distance of zero corresponded to the tip of the cerci being touched by
the piston. Positive and negative values for escape distances corresponded to
air- and touch-evoked responses, respectively. We normalised escape distances
to the total body length of the cricket to provide a more ecologically
relevant measure of cricket escape performance. This measurement indicates how
many cricket body lengths remain between the cricket and the mimicked spider
before the cricket escapes (Fig.
3). All image analyses were performed using R (R development core
team 2004).
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Statistical analyses
Log-transformed proportions of various types of escape behaviours
(Table 1) were analysed using a
Tukey-type multiple comparison test (Zar,
1998). Log-transformed escape distance data
(Table 2) were analysed using
two-way repeated-measures ANOVA, in which `instar' and `attack velocity' were
the first and second factors. In cases of statistically significant changes,
data were further analysed using a post hoc Fisher's least
significant difference (LSD) test. Data were considered significant for
P values less than 0.05. All statistical and image analyses were
performed using R.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Cricket escape distance
We detected significant differences in normalised cricket escape distance
among instars for all three piston velocities in both air- and touch-evoked
escapes (Fig. 3,
Table 2). Post-hoc
comparisons revealed that adults had lower air- and touch-evoked escape
distances than juveniles (I and II), for all attack velocities. Interestingly,
we observed an increase in interindividual variability of escape distance with
cricket development: few adult crickets can react as quickly as juveniles
after being touched by the piston and most adults have a two- to fivefold
increase in normalised escape distances. This ontogenic difference in escape
distance was more pronounced for air-evoked escapes: the greatest escape
distances to wind signal (up to 2.3 times the cricket body length) were always
observed in juveniles for all three piston velocities
(Fig. 3). However, this result
was a consequence of the normalisation of escape distances to cricket body
length. When applied to absolute escape distance, the wind-evoked response was
the same among age classes (ANOVA, F=1.9361, P=0.1766, data
not shown). No effects of piston velocity on the escape distance of crickets
for any type of response were detected
(Table 2).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Gnatzy,
1996). However, our field study further describes various types of
predator signals. We observed that most crickets escaped running predator
signals only after physical contact and not by using their air-detection
system, as it is generally assumed. This result was observed for all tested
piston velocities and suggests a crucial, but previously disregarded, role for
cercal touch perception in cricket escape performance. Crickets can rely on
powerful legs to escape predators and this may explain why they wait until the
last moment to initiate a jump. This late reaction may explain why most
crickets do not consistently achieve escape angles between 60 and 90° from
the source of danger (e.g. 60–90°) (see
Tauber and Camhi, 1995) before
jumping. The prominent role of touch-sensing for escaping from predators may
have been reinforced by the field conditions of the experiment. Air signals
from a predator may be barely detectable and poorly reliable in the presence
of background noise created by wind turbulence, a feature that has been
observed in foraging bats (Jones and
Rydell, 1994). Moreover, touch-sensing may be more efficient than
air-sensing in detecting predators (such as spiders) at close range in leaf
litter.
Ontogeny of escape performance in an evolutionary ecological context
Most studies on the development of performance of traits related to escape
behaviour have focused on locomotion, generally reporting that adults have
higher or similar absolute capacities than juveniles [e.g. lizard speed
(Irschick, 2000), mammal speed
(Trillmich et al., 2003)].
However, Gibb et al. (Gibb et al.,
2006) proposed that the development of the escape response in
Teleost fish would decrease as juveniles become larger, as a result of
biomechanical constraints in body shape. Measurements of the escape distance
in crickets lead us to similar conclusions: escape performances in juveniles
were higher than those in older instars. This increase in the escape distance
for juveniles was in most cases related to a lower reaction distance after
being touched by the piston: they respond faster than adults to an immediate
danger. The decline in the escape performance for all tested speeds and for
both escape types, despite strong differences in stimulus transmission to the
sensory structures, is striking and calls for further interpretation in terms
of neural control processes related to the age of the animal.
The negative relationship between body size and escape performance may have
important implications in an evolutionary and ecological context. For
instance, optimality theory suggests that the behavioural response of an
individual in response to a predator is influenced by the risk of predation
(Ydenberg and Dill, 1986).
Although juvenile crickets forage in the same environment as adults and are
faced with the same predators, they suffer higher rates of mortality, partly
because their smaller size makes them more vulnerable to predators
(Dangles et al., 2006a). An
increase in absolute size allows crickets to reach a size-refuge, the size at
which they become too big to be caught by most wandering predators. This
hypothesis is supported by the greater proportion of walking responses in
adults than juveniles; it is also supported by a previous experiment reporting
more frequent hiding behaviour in juvenile crickets than in adults exposed to
predators (Dangles et al.,
2006a). A broad range of morphological, physiological, behavioural
and ecological changes through ontogeny affect performance
(Irschick, 2003); however, the
specific concept of size-refuge has seldom been considered by functional
ecologists [for an exception, see Wainwright
(Wainwright, 1996)]. We expect
that the concept of size-refuge would improve our understanding in the
development of performance, given its importance in community and population
ecology theories [see Aljetlawi et al.
(Aljetlawi et al., 2004) and
references therein]. This is another reason to move swiftly towards more field
experiments carried out in ecologically relevant settings.
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