Escape behavior and escape circuit activation in juvenile crayfish during preypredator interactions
Department of Biology, Georgia State University, Atlanta, GA 30303, USA
* Author for correspondence (e-mail: biojhh{at}langate.gsu.edu)
Accepted 22 March 2004
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Summary |
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Key words: crayfish, Procambarus clarkii, dragonfly nymph, Anax junius, predator, prey, escape
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Introduction |
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Previous studies that examined predation on crayfish reveal little detail
of the actual escape behavior and were mostly concerned with ecological
implications (Dye and Jones,
1975; Stein and Magnuson,
1976
; Stein, 1977
;
DiDonato and Lodge, 1993
;
Garvey et al., 1994
;
Hill and Lodge, 1994
;
Söderbäck, 1994
;
Blake and Hart, 1995
;
Correia, 2001
). These studies
were either carried out in the field or in large test chambers (i.e. outdoor
pools) where interactions between large predators (e.g. smallmouth bass) and
crayfish were observed. In these conditions, it was possible to determine when
crayfish escaped from an attack but it was not possible to determine which
type of tail-flip the crayfish used to escape.
Dragonfly nymphs are opportunistic aquatic predators that hunt other
invertebrate larvae including conspecifics
(Merrill and Johnson, 1984;
Wissinger, 1989
;
Johansson and Johansson, 1992
;
Wissinger and McGrady, 1993
),
tadpoles (McCollum and Leimberger,
1997
; Barnett and Richardson,
2002
) and small fish (Crumrine
and Crowley, 2003
). The predatory strike of dragonfly nymphs is
based on hydraulic mechanisms. The animals close the anal valve and contract
the abdominal dorso-ventral muscles to generate a rapid increase in hemolymph
pressure that is followed by labial extension
(Pritchard, 1965
;
Olesen, 1972
). The fast
movement of the labium is accomplished by storing muscular energy during the
preparatory period of the strike (Tanaka
and Hisada, 1980
; Kanou and
Shimozawa, 1983
).
We found that dragonfly nymphs reliably attack juvenile crayfish and consume them after capture. Moreover, both animals are small enough to be tested in an aquarium that allows high-speed video recordings in combination with recordings of electric field potentials by use of bath electrodes. Therefore, they represent an ideal model for studying the details of preypredator interactions in the laboratory. For 50 years, in the absence of any concrete behavioral evidence, it was assumed that the escape circuits in crayfish are activated in response to attacks from predators. Here, we test this hypothesis for the first time by measuring the activity of the escape circuits in response to attacks from natural predators.
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Materials and methods |
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In a series of 41 single experiments, one crayfish and one dragonfly nymph were paired in a small test chamber (8x4.5x4 cm) filled with deionized water (height, 3 cm). None of the animals was used in more than one experiment. Animals were size matched for each experiment, with all crayfish (mean ± S.D., 2.1±0.2 cm; range, 1.72.6 cm; measured from rostrum to telson) being within 5059% of the size of the dragonfly nymph (mean ± S.D., 3.9±0.4 cm; range, 3.14.7 cm; measured from tip of head to end of abdomen). Two lights were directed towards the test chamber to provide sufficient illumination for the high-speed video recordings. All animals were checked for physical intactness before the experiments and no crayfish molted within four days prior to or two days after the experiment. In a few experiments, the dragonfly nymphs did not attack the crayfish within 20 min after both animals were introduced to the test chamber. The animals were removed and no data were included in the analysis. Results from three experiments (7%) were excluded from the analysis because the video- and electrical recordings were not clear. Thus, a total of 38 experiments (i.e. attacks) were eventually used for analysis and statistical procedures. Non-parametric tests (Jandel SigmaStat® 2.0 and GraphPad Prism® 4.0) for independent data [KruskalWallis one-way analysis of variance (ANOVA) on ranks, MannWhitney rank sum test and Fisher's exact test] were applied for statistical comparison.
Field potentials from the aquarium bath were recorded with a pair of silver wire electrodes (1 mm outer diameter, insulated except at the tips) placed at either end of the test chamber. The signal was AC-coupled and amplified (1000x; A-M Systems, Sequim, WA, USA), displayed on an oscilloscope and simultaneously recorded on a personal computer with Axoscope software (Axon Instruments, Union City, CA, USA).
The behavior of the animals was taped with a high-speed video camera (5 ms frame-1; JC Labs, San Mateo, CA, USA) from above and the side by means of a mirror angled at 45° from the base of the aquarium. Another mirror reflection of the oscilloscope trace in the bottom half of each video frame was used to correlate the recorded behavior and the electric field potentials recorded by the oscilloscope as well as the computer. The camera was connected to a video-recorder as well as a monitor, and data were stored in S-VHS format. The recordings were started shortly before the animals were introduced into the test arena and stopped some time after an attack by the dragonfly nymph had taken place. The behavior of the prey and predator were also recorded in a larger arena using a digital video camera (Canon XL1-S). All video recordings were digitized by use of Adobe Premier® and Dazzle* Digital Video CreatorTM, and single frames were used for analysis and illustrations.
Video- and field potential recordings were also used to monitor attacks from isolated dragonfly nymphs directed towards mock prey by use of a Puritan® cotton-tipped cleaning stick (length, 15 cm) or a small piece of black tape on a string moved randomly in front of them.
Under the same experimental conditions (but with a video-camera side view
only) we also measured the response latencies of individual escape tail-flips
generated by six previously isolated crayfish of a similar size
(2.4±0.2 cm) as used during preypredator interactions. The
animals were stimulated to tail-flip with a handheld glass probe by tapping
them to the front or rear at different intensities. Sharp taps were
administered to evoke giant mediated tail-flips and gentler taps to evoke
non-giant tail-flips (cf. Herberholz et
al., 2001). The latency of each response was measured by counting
the video-frames between the contact of the probe on the crayfish's body and
the activation of the respective escape behavior displayed as the initial
movement of the crayfish. A minimum of five tail-flips of each type was
collected from each animal.
Identification of a tail-flip depended on the correlation between the
high-speed video recording of the tail-flip and the simultaneously recorded
field potential. Electrical recordings from the bath electrodes warrant
identification of LG- or MG-mediated tail-flips by their large, phasic motor
giant (MoG) neuron potentials and the immediately preceding LG or MG neuron
action potentials (Herberholz et al.,
2001). The identification of the giant mediated tail-flips,
however, was somewhat complicated in our study because the nymphs produced
muscle potentials during attacks that were big enough to be recorded by the
bath electrodes. These potentials started shortly before an attack and passed
into the measured potentials from the crayfish tail-flip activity.
Consequently, the giant neuron spikes were rarely identifiable in our
recordings. The MoG potentials, however, were unaffected by the nymph's signal
and were always of large amplitude. Thus, we felt confident in identifying the
giant mediated tail-flips from this characteristic feature. MG-evoked
tail-flips have a larger amplitude and a shorter duration of the MoG potential
and can be used to discriminate between the two giant mediated tail-flips (cf.
Herberholz et al., 2001
). In
addition, single frame analysis of the high-speed videography allowed us to
distinguish between the two giant mediated tail-flips (upward and backward
movements are indicative of LG and MG tail-flips, respectively). Non-G
mediated tail-flips cannot be discriminated behaviorally from giant mediated
tail-flips, but their electrical recordings lack the large MoG potentials and
consist of much smaller and more erratic fast flexor (FF) muscle potentials
only (cf. Herberholz et al.,
2001
).
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Results |
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Field potential recordings
All known and previously described types of escape tail-flips were evoked
by attacks from the dragonfly nymphs. The muscle potentials generated during
these escape responses were recorded with a pair of bath electrodes in the
test chamber. Fig. 2A
illustrates the combination of an electrical recording and the simultaneously
recorded video sequence during an MG-mediated escape tail-flip produced by the
crayfish in response to a frontal attack from the dragonfly nymph. The
recording from the bath electrodes is shown on top. Examples of the
corresponding video frames showing the behavior of the animals (top view and
side view via mirror image) as well as the corresponding oscilloscope
trace for each frame are shown on the bottom. For better illustration, the
reflected oscilloscope traces were flipped horizontally to match with the
electrical recordings sampled on the computer. The first two frames show parts
of the nymph's attack with the opening of the labial palps and the extension
of the labium, respectively. The third frame shows the moment when the escape
behavior is initiated shortly after the labium hit the body of the crayfish.
The last frame shows a later part of the escape behavior with the crayfish
being propelled back and away from the predator.
|
The muscle potential produced by the predator was recorded by the bath electrodes and always preceded the signal generated by the crayfish (Figs 2A, 3). This signal usually started with small deflections when the nymphs opened the palps on either side of the labium that became larger when the labium was extended during the strike (Fig. 2A). The mean duration of the predators' muscle potentials was 33.6±7.9 ms (1149 ms, N=38; measured from the beginning of the signal to the start of the potential produced by the crayfish's escape circuits). The durations did not differ significantly for the three different types of tail-flips that were elicited (P>0.05; KruskalWallis one-way ANOVA on ranks). The mean duration of the extensions (measured by counting the video frames between the onset of the movement of the labium and the moment when the target was hit) was 14.8±3.7 ms (N=38) and was much shorter than the actually recorded muscle potentials. Since each video frame represents a period of 5 ms, the calculated response latencies from the measured number of frames are only a demonstration of the time window in which the behavior occurred. Moreover, the measured extensions did not include the initial part, i.e. the preparation of the strike when the nymphs opened the labial palps.
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The signal of the predator was also measured in eight isolated nymphs that were stimulated to launch an attack against mock prey. We found that the signal duration in these experiments averaged 46.5±5.9 ms (N=17), more than 10 ms longer than during preypredator interactions (Fig. 2B). Thus, in the electrical recordings taken while the nymphs attacked crayfish, the later part of the signal emitted by the dragonfly nymphs was masked by the larger signal generated by the crayfish.
Fig. 3 shows examples of three types of recorded muscle potentials that represent the three different types of tail-flips. The recordings from MG- and LG-mediated tail-flips both show the large and phasic MoG potentials as well as the following FF muscle activity (Fig. 3A,B). The Non-G-mediated tail-flip produced a very different crayfish response consisting of a much smaller and less phasic potential that can be attributed to FF muscle activity only (Fig. 3C). Extensor muscle potentials that usually follow the FF muscle potentials with some delay were small and rarely identifiable in our recordings. The arrowheads shown above the traces indicate the beginnings of the predators' muscle potentials.
Initial escape responses to an attack
Each single attack from the dragonfly nymph was answered with a tail-flip
escape response by the crayfish (100%, N=38). The attacks were
directed to most parts of the crayfish's body with the majority aimed at the
head and thorax and fewer directed towards the abdomen
(Fig. 4A). Rarely was the
attack directly aimed at the appendages (i.e. claws, walking legs, antennae,
antennules). In some cases, however, the nymph hit appendages first before the
strike was passed on to the body. Most attacks evoked activity in the MG
neuron (63%) and less evoked activity in the LG neuron (24%;
Fig. 4B). Only five attacks
(13%), all directed to the front of the animal, were answered by
Non-G-mediated tail-flips that were identified by their characteristic muscle
potential recordings (Fig.
4B).
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Fig. 5 shows the distribution of hits to the crayfishs' bodies that excited the three different escape responses. The round circles indicate the position of the center of the labium on the crayfish's body. A schematic of the frontal part of the labium is shown to illustrate the size relation. Arrows around the crayfish demonstrate the direction of the attack (i.e. the position of the dragonfly nymph). A strong correlation between the evoked tail-flip escape response and the target of the strike can be seen: MG- and Non-G-mediated tail-flip responses were only elicited by attacks to the front part of the crayfish (head and thorax) while attacks to the abdomen evoked LG-mediated escapes only. The position of the nymph, however, varied with regard to the evoked responses.
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The response latency of the different escape tail-flips was measured by
counting the video frames between the contact of the labium on the crayfish's
body and the activation of the respective escape behavior displayed as the
initial movement of the crayfish. These latencies
(Fig. 6A) were significantly
different for the three different types of tail-flips (P0.01;
KruskalWallis one-way ANOVA on ranks). The responses triggered by
activity in the Non-G circuit were significantly slower than responses
generated by activity in the MG or LG neurons (P
0.01 and
P
0.05, respectively; MannWhitney rank sum test). When
compared with escape latencies measured in isolated crayfish (N=6,
n=144) of the same size that were stimulated with a handheld probe,
the latencies for MG-mediated tail-flips (predator, 10.0±1.5 ms; probe,
9.7±1.1 ms) and LG-mediated tail-flips (predator, 11.7±2.5 ms;
probe, 12.6±1.3 ms) were found to be almost identical under both
conditions. However, latencies for Non-G tail-flips were significantly shorter
(P
0.01; MannWhitney rank sum test) during predator-evoked
escapes (predator, 16.0±2.2 ms; probe, 57.2±5.7 ms;
Fig. 6A).
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Overall, the initial tail-flip response proved to be a successful escape mechanism for juvenile crayfish to prevent predation from the dragonfly nymphs. In 45% of all cases (17 of 38), the initial tail-flip response catapulted the crayfish out of reach before the predator was able to restrain the prey. In all other cases (55%), the nymph caught the crayfish with the sharp labial palps, pulled it towards the body and started using its mouthparts to consume it. Since the neural escape circuits are always excited in these cases and the escape behavior is initiated before the crayfish is restrained, we were able to identify the type of initial tail-flip response in every case by combining the measurements from the bath electrodes with our video recordings.
The two giant mediated types of tail-flip escapes were found to be equally successful in preventing capture (Fig. 6B). The LG-mediated tail-flips provided an escape rate of 44% (four of nine), while MG-mediated tail-flips had an initial escape rate of 50% (12 of 24). Only one of five (20%) of the Non-G-mediated tail-flips, however, was successful in preventing capture (Fig. 6B).
Additional escape behavior after capture
Once caught, the crayfish often produced a series of Non-G-mediated
tail-flips to escape from the nymph's grip (mean ± S.D.,
4.5±3.8). Only in two cases did the crayfish not generate additional
tail-flips after capture and in both cases the animals were killed and
consumed.
Fig. 7A shows a trace recorded by the bath electrodes that displays the muscle potentials produced by predator and prey during and after the attack. A giant mediated tail-flip was generated first as an immediate response to the attack but was followed by three non-giant mediated tail-flips after the animal was captured. Although the subsequent tail-flips did not free the crayfish from the dragonfly nymph in this case, additional tail flipping after capture was generally very effective and produced many additional escapes with or without inflicted injuries (14 of 19; 74%). None of the crayfish that escaped injured (six of 21; 29%; typically, loss of a claw or a walking leg) died as a result of the injury.
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The success of a captured animal's escape attempts depended on where the animal was attacked and held. Animals captured by frontal attacks were significantly more likely to escape than animals captured by abdominal attacks (81% and 20%, respectively; P<0.05; Fisher's exact test). That increased frequency of escape was associated with a greater number of Non-G tail-flips (Fig. 7B). Successful frontal attacks triggered unsuccessful MG or unsuccessful Non-G tail-flips that were followed by a high number of subsequent Non-G tail-flips (mean ± S.D., 5.4±4.5 and 5.0±2.2, respectively), and these additional tail-flips led to escape in 91% (10 of 11) and 75% (three of four), respectively, of all cases in which they were executed (Fig. 7B). Successful abdominal attacks that triggered unsuccessful LG tail-flips were followed by only 1.8±1.9 Non-G tail-flips, and these achieved an escape rate of only 25% (one of four; Fig. 7B). In these cases, the dragonfly nymphs caught the crayfish by closing the sharp labial palps around the tail or abdomen, which prevented the crayfish from executing non-giant mediated tail-flips or generating full force during non-giant mediated tail-flips. Consequently, only one crayfish that initially produced a LG-mediated tail-flip in response to the attack escaped after being caught. The differences in numbers of additional non-giant mediated escapes after MG-, LG- and Non-G-initiated tail-flips did not reach statistical significance (P>0.1; KruskalWallis one-way ANOVA on ranks). They do, however, explain the high mortality rate of captured crayfish that initially tried to escape by LG-mediated tail-flips (see below).
Unsuccessful escapes and mortality rates
Only 18% (seven of 38) of all attacks from the dragonfly nymphs were fatal
with the crayfish being killed and consumed. Crayfish that initiated an escape
with MG-mediated tail-flips and were captured (50%) still suffered a low
overall mortality rate of 8% (two of 24) because of the high number of
successful Non-G-mediated tail-flips they generated after capture. Likewise,
the unsuccessful Non-G-mediated tail-flips (80%) produced by the crayfish to
avoid capture were compensated for by the high number of successful
Non-G-mediated tail-flips that followed capture and resulted in a 20% (one of
five) mortality rate. Crayfish that attempted LG-mediated escapes and were
captured (56%), however, experienced a high mortality rate of 44% (four of
nine), mostly because subsequent Non-G-mediated tail flipping was
disabled.
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Discussion |
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The bath electrodes were sensitive enough to record field potentials
generated by the predator before and during its attack. The muscle potentials
produced by the dragonfly nymphs in our experiments showed an increase in
amplitude over time, reflecting previously reported recordings made with
implanted electrodes (Tanaka and Hisada,
1980). The potentials recorded with bath electrodes were much
shorter, however, than described from electromyograms, and the largest
deflections were observed during the extension of the labium, i.e. after the
onset of the strike. Only the extensor and the adductor muscles of the labium
are active at this time (Tanaka and
Hisada, 1980
), and the later part of the recorded field potentials
may therefore be attributed to activity in these muscles. On the other hand,
it seems unlikely that these small muscles in the labium solely account for
the large potentials recorded with the bath electrodes during labial
extension. Possibly, the dorso-ventral muscles that create the increase in
hydrostatic pressure are in part responsible for these large potentials and
are active longer than previously reported
(Olesen, 1972
;
Tanaka and Hisada, 1980
).
Most dragonfly attacks were directed at the head and thorax of the crayfish
(Figs 4A,
5), perhaps because the
crayfish's exploratory tour of the aquarium led it to approach the stationary
predator. Each strike was then answered by an attempted tail-flip escape. As a
consequence of the strong and phasic nature of the predatory strike, most of
the evoked tail-flips were mediated by activity in the giant neurons (Figs
4B,
5). The type of giant mediated
escape response depended on the target of the attack but not on the position
of the attacker. LG-mediated escapes were only evoked by strikes to the
abdomen, whereas MG-mediated escape tail-flips were only evoked by strikes to
the head and thorax (Fig. 5).
This is consistent with earlier descriptions of the receptive fields of LG and
MG as being non-overlapping and restricted to the abdomen and cephalothorax,
respectively (Wine and Krasne,
1972). A few attacks to the anterior part of the crayfish's body
elicited Non-G-mediated tail-flips (Figs
4B,
5). We found no apparent
differences in target, position of the predator or physical parameters of the
strike that would distinguish these attacks from the ones that evoked
MG-mediated escapes. Nonetheless, the Non-G-mediated tail-flips had
significantly longer response latencies than the giant mediated escapes
(Fig. 6A). However, the Non-G
latencies were shorter than those measured in earlier studies that evoked
tail-flips by tactile stimulation with a tapping rod
(Wine and Krasne, 1972
;
Reichert and Wine, 1983
;
Kramer and Krasne, 1984
). They
were also shorter than Non-G latencies measured in this study after
stimulation with a glass rod under the same conditions in animals of similar
size, whereas latencies for MG- and LG-mediated tail-flips did not differ
whether evoked by nymph attacks or by a tapping rod
(Fig. 6A). The longer latencies
for Non-G tail-flips have been attributed to the `voluntary' nature of the
escapes in which the animals make decisions about the direction and angle of
the response before the tail-flip is executed
(Wine and Krasne, 1972
;
Reichert and Wine, 1983
). The
processing time required to set up the Non-G system was therefore considered
to account for the long response latencies after stimulation
(Reichert and Wine, 1983
). The
surprisingly short response latencies for Non-G-mediated escapes reported here
during predator attacks reveal an interesting possibility; the Non-G system
may be primed by the perception of the approaching predator (e.g. the labial
extension), thereby reducing the latency of the Non-G response that follows
the actual physical contact. However, because of the low number of observed
Non-G tail-flips in response to predator attacks and the relatively low
temporal resolution of our high-speed system, additional experiments are
required to test whether crayfish actually use sensory information provided by
the predator to prepare the Non-G escape response prior to the tactile
stimulation.
The crayfish used in our study were successful in employing tail-flip escapes to prevent capture and so experienced low mortality rates. Crayfish that are smaller or larger in size relative to the predator, however, may experience different mortality rates during interactions with dragonfly nymphs. Non-G tail-flips were less successful in preventing capture than giant mediated tail-flips (Fig. 6B), probably because of the longer response latencies measured for Non-G-mediated escapes as compared with giant mediated escapes (Fig. 6A), and because Non-G tail-flips generate less thrust than giant mediated tail-flips. Although not efficient for initial escape, activation of the Non-G system was common after capture (Fig. 7A) and generated many additional escapes (Fig. 7B). These additional tail-flips were predominantly used after unsuccessful MG- and Non-G-mediated escapes (Fig. 7B) but rarely produced after initial LG tail flipping. Attacks that elicited LG-mediated escapes were always directed to the rear of the crayfish, and closure of the labial palps around the tail or abdomen prevented the crayfish from executing Non-G tail-flips or generating full force during attempted Non-G tail-flips.
Tail flipping without giant fiber activity is considered the early
condition of escape in crustaceans
(Heitler et al., 2000). We
found that Non-G-mediated tail-flips in juvenile crayfish are ineffective for
escaping the fast and precise strikes generated by predators such as dragonfly
nymphs. The coexistence with predators delivering phasic stimuli during
attacks may have led to the evolution of the giant fibers that enable
powerful, short-latency escape responses. Activation of either the MG or LG
neuron generates rapid and powerful tail-flip responses that allow crayfish to
escape from sudden attacks. However, the enduring importance of the ancestral
form of escape is still apparent: although not very successful during initial
escapes, the Non-G-mediated tail-flips are of great importance for the overall
survival, accounting for many additional escapes after capture.
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Acknowledgments |
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Footnotes |
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