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First published online August 3, 2006
Journal of Experimental Biology 209, 3226-3233 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02368
Exploring with damaged antennae: do crayfish compensate for injuries?
Department of Zoology, University of Melbourne, Parkville, Victoria, 3010, Australia
* Author for correspondence (e-mail: blairp{at}unimelb.edu.au)
Accepted 5 June 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: crustacea, haptic systems, learning, touch
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Fine-Levy and Derby, 1999; Thoms and
Sheldon, 2000; Grasso and
Basil, 2002). The capacity to explore in the dynamic conditions of
the zone may provide selective advantage for many organisms. Advantageous
adaptations for such activity are likely to rely heavily on non-visual stimuli
(Kaplan et al., 1993) because,
in the absence of visual input, other modalities become more important. Sound,
chemical and tactile (touch) cues can be used to collect information
(Webster and Weissburg, 2001).
Of these, touch information and chemosensory input are likely to play a major
role in exploratory behaviour (Taylor,
1975; Tautz et al.,
1981).
Many adult crustaceans are benthic. Much is known about how they interpret
chemical cues in their environment (e.g.
Hazlett, 1971;
Reeder and Ache, 1980;
Derby and Atema, 1982;
Beglane et al., 1997;
Derby and Steullet, 2001;
Kraus-Epley and Moore, 2002;
Cate and Derby, 2002a;
Cate and Derby, 2002b). Less
is understood about how they use tactile information. Research in this field
has focused on how it is used for prey location. Zeil and colleagues
(Zeil, 1985) discovered that
both sighted and blind crayfish use their antennae to locate small stationary
objects, such as mussel shells. Crayfish also orient themselves to swimming
fish prey with their antennae (Breithaupt
et al., 1995). Tactile cues are likely to be used for more
behaviours than these, such as shelter search and territory exploration, but
there is limited information on such exploratory activities [shelter
(Alberstadt et al., 1995),
exploration (Basil and Sandeman,
2000; Patullo and Macmillan,
2006)].
The second antennae provide much of the touch information available to
decapod crustaceans (Tazaki,
1977; Vedel,
1985). In most crayfish, the antennae are flexible, tapered and
almost as long as the animal's body (e.g.
Sandeman, 1989). Each antenna
consists of five short proximal segments (the base) supporting a long,
multi-segmented flagellum (Tazaki and
Ohnishi, 1974; Sandeman,
1985; Zeil et al.,
1985). The antennae assess position, movement, direction and
velocity of one segment relative to the next
(Hartman and Austin, 1972;
Sigvardt, 1977;
Zeil et al., 1985;
Sandeman and Varju, 1988).
Tactile information appears to be derived mainly from the active movement
of sensory appendages. Walking crayfish wave their antennae back and forth
through horizontal angles of 100° or more relative to the long axis of the
body (Sandeman and Wilkens,
1983; Zeil et al.,
1985; Breithaupt et al.,
1995). This active movement resembles that of other tactile
systems that require active touch or tactile scanning
(Gibson, 1962;
Zeil et al., 1985). Tactile
scanning requires mobility of the sense organ, and the capability to discern
the position of the sense organ in relation to the body
(Sandeman, 1985). A sense
organ with these two properties allows an animal to estimate the angle of the
sense organ relative to its body, and the distance between the body and
objects in its path. This information can then be combined or compared
(McMahon et al., 2005), and
allows the animal to form an image of the three-dimensional layout of their
environment (Zeil et al.,
1985). This is particularly relevant when animals explore new
terrain (Basil and Sandeman,
2000; Patullo and Macmillan,
2006).
Given that the antennae are important in forming an image of the
environment and in other behaviours, it could be advantageous for them to
remain functional for the entire life of the animal
(Harrison et al., 2001).
However, the proximity of antennae to danger
(Bovbjerg, 1956), and their
mobility, makes injury likely. Crayfish, and other crustaceans, have the
capacity to regenerate antennae (Harrison
et al., 2001), but it takes time for an injured appendage to
become indistinguishable from the original, sometimes more than 6 months
(Harrison et al., 2001;
Hartman and Cooper, 1994). It
is therefore likely that for periods in an animal's life its sensory and
locomotory appendages are not intact.
Individuals with incomplete, or non-functional, sensory appendages may be
disadvantaged. How crayfish accommodate such situations is not fully
understood. There is some evidence that reduced tactile information changes
their behaviour. Crayfish of the species Cherax destructor with one
flagellum denervated favour searching toward the intact side
(McMahon et al., 2005). When
both flagella are severed at the base, the animals no longer walk close to
surfaces that provide tactile information
(Basil and Sandeman, 2000).
These results support the hypothesis that the antennae are the primary tactile
appendages used in exploration so that any damage to them could be
disadvantageous.
Crayfish may be able to offset lost tactile input by compensating with
information from other sources besides the antennae in the same way that other
arthropods compensate for lost appendages until they have regrown
(Blazis and Grasso, 2001).
Derby and Steullet proposed that multiple sensors act to maintain the function
of some sensory systems in the face of damage and compensate for
non-functioning developmental sensor stages
(Derby and Steullet, 2001). It
is largely unknown whether compensatory mechanisms operate in crayfish tactile
systems. Mechanoreceptive setae, which cover almost all body surfaces,
including the chelae and the dactyls
(Tazaki and Ohnishi, 1974;
Tautz and Sandeman, 1980;
Solon and Kass-Simon, 1981),
may provide alternative sources of information. A familiar environment could
also help. Crayfish are capable of learning local topography in a short period
of time (Basil and Sandeman,
2000; Shuranova et al.,
2005). Individuals that know an area may therefore be able to
navigate through it successfully on subsequent visits with less than normal
tactile information.
The goal of this study was to provide insight into how crayfish with injured antennae behave and whether or not they can compensate for the lost information. Appendages were ablated to simulate damage that occurs in the wild. Four objectives were addressed: (1) how the complete or partial loss of antennae affects exploratory behaviour; (2) whether search strategy changes during repeated exposure to the same environment after damage to the antennae; (3) whether prior experience in an environment can compensate for exploration with damaged antennae; and, (4) whether other appendages can provide tactile information to compensate when both antennae are damaged.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Apparatus
Experiments were conducted in a tubular T-maze constructed from PVC pipe
(10 cm diameter). This apparatus is briefly described here, and in more detail
by McMahon et al. (McMahon et al.,
2005). Two 55 cm long side arms were joined to a 120 cm long
entrance arm with a T-joint, and capped
(Fig. 1). A 3 cm wide cut-out
was made in the top of the maze. Crayfish placed in the base of such a maze
navigate their way to the top and turn into one of the arms
(McMahon et al., 2005).
Individuals could simultaneously touch both side walls of the maze with their
antennae and walked up the centre.
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Procedure
Operations
Four experiments were conducted with combinations of operated and
unoperated animals. Other research has taken a similar approach to investigate
the control of decapod behaviour (e.g.
Beglane et al., 1997;
Basil and Sandeman, 2000;
McMahon et al., 2005). Tactile
information available to crayfish was systematically altered by the removal of
antennal flagella and chelae. The ablations simulated damage that occurs in
the wild, e.g. severing of an antenna by an opponent's chelae during a fight
or autotimising a cheliped to escape. Crayfish were anaesthetised by immersion
in crushed ice for 30 min prior to surgery. The location of the operation and
the timing of the maze testing in relation to the surgery are outlined below
and in Figs 1 and
2.
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Animals were randomly assigned one of four ablation types. (1) Antennal
base. One flagellum was severed at the base between the first and tenth
annuli. This removed the flagellum but left the basal proprioceptors intact.
The animal received no mechanosensory input, but position information was
still available from the basal segments. (2) Antennal midpoint. The ablation
occurred between the 50th and 60th annuli distal to base. This standardised
the amount of flagellum animals had, and thus reduced, in a controlled manner,
the amount of tactile input the animal received. It resulted in an antenna
that was shortened to approximately 25 mm in length (intact antennae are about
60 mm for these sized crayfish). (3) Chelae. Each chela was held immobile and
a pair of fine scissors was used to cut into the animal's exoskeleton
immediately distal to the autotomy plane, at the seam between the basis and
the ischium (see Wood and Wood,
1932; Bliss, 1960;
McVean, 1975). This caused the
animal to autotomise its chela, and allowed the wound to seal and heal quickly
and cleanly. (4) Sham. To control for any operational effects, groups of
crayfish were treated identically to other operated animals but the appendages
were not severed.
For experiments in which only one of a pair of appendages was ablated, individuals were randomly assigned to left or right side treatment. Crayfish were allowed 1 day to recover before a trial in the T-maze.
Trials in the maze
Trials commenced approximately 30 min after the onset of dark, and
continued for 3-4 h. Crayfish are mainly nocturnal and there is evidence in
some species that this is the most active period
(Page and Larimer, 1972). Red
light illuminated the experimental room (fluorescent tube with red filter,
light levels of less than 1 lux at maze level). This allowed the experimenter
to view animals and facilitated filming, but prevented animals receiving
visual cues. Behavioural tests show that crayfish behaviour is unaffected by
movement at such light levels (McMahon et
al., 2005).
A crayfish was removed from its housing tube by net and placed in an empty
plastic container (20x20x10 cm) for 6 min. It was then tipped into
the base of the T-maze (starting point, see
Fig. 1). Observations began
when the rostrum of the crayfish crossed the starting point in a forward
direction. Trials ended when the rostrum crossed the end line located 5 cm
from the junction in one of the side arms (end line, see
Fig. 1). Previous research
showed that once a crayfish crossed this point it remained in that arm
(McMahon et al., 2005).
Animals were given 10 min to complete the task. Individuals that did not reach
the end of the maze in that time were noted but excluded from analysis.
Following each trial, the maze was cleaned twice with a high-pressure hose and
refilled.
Experiments
Experiment 1
To examine how complete and partial loss of a flagellum affects behaviour,
two ablation points were used: basal and midpoint. Forty five crayfish were in
each of these treatment groups.
Experiment 2
To investigate whether recent experience in an environment before sensory
loss allows an animal to compensate for subsequent loss of antennae, animals
were run through the maze prior to the operation. Two groups of 40 crayfish
were assigned to a treatment and control. The crayfish were run once in the
T-maze 5 days prior to their operation or sham treatment. Operated animals had
an antenna severed at the base and control crayfish remained intact.
Experiment 3
To determine whether repeated exposure to the same environment after
ablation would allow animals to compensate for lost antennal information, two
groups of 45 crayfish were run in the maze seven times. `Basal' animals had
one flagellum severed at the base and control animals remained intact. Animals
were run through the T-maze after the recovery period and then again 5, 10,
15, 20, 25 and 30 days post operation.
Experiment 4
To test whether information from other appendages is used by crayfish to
compensate for reduced antennal input, chelipeds were ablated at the same time
as both antenna were ablated. The chelae were selected because they have
tactile receptors and are positioned on either side of the body so they may
provide directional information in the maze. Three experimental groups of 45
animals were used: no chelae, one chela, control. The control group was
handled to simulate the ablation of two chelae, whereas the one-chela group
had one chela severed, and the no-chelae treatment group had both chelae
ablated.
Data analysis
In all experiments, the number of animals that turned in different
directions (left or right arm) was compared. For operated animals, the
direction turned was referenced to the ablated flagellum to give a score of
either toward or away from the intact side. These binomial data were analysed
using Yates corrected 
2 tests, as there were only two possible
outcomes (Sokal and Rohlf,
1995). Previous experiments with large populations of intact
animals show that crayfish display unbiased turn behaviour in this maze
(McMahon et al., 2005). Values
were therefore compared to an expected outcome of an equal number of turns
into the two arms. Groups of control animals were run throughout the
experiments to confirm this and ensure that some seasonal or sample bias was
not present. A Wilcoxon sign rank test was performed on the repeated
experience data to see if the ablated animals turned consistently in the same
manner as the shams (Sokal and Rohlf,
1995). Time (s) spent travelling to, and in, the junction were
compared between treatments in each experiment with ANOVA or two sample
t-tests. Data were compiled using Microsoft Excel 2000 and analysed
in Minitab v13.20 or Systat v11. P-values of less than 0.05 were
considered significant.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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2=0.013, P=0.909). These results verify that intact
crayfish use a random search strategy in this maze environment
(McMahon et al., 2005) and
confirm the control status of this cohort of animals.
Partial or total antennal ablation
Animals with one base-ablated antenna held the intact antenna ahead of
them, the base of the severed antenna also appeared to be held ahead. Crayfish
with one antenna ablated at the base displayed a significant bias in the
direction turned at the junction. Thirty-four crayfish turned toward their
intact antenna and 10 away (2=12.023, P<0.001).
Individuals with one antenna ablated at the midpoint displayed no bias in
their turns. Fifteen animals turned away from their intact side, whereas 27
turned toward that side (2=2.881, P=0.089).
One traverse of the maze prior to antennal ablation
Prior to the operation, both groups of animals displayed no turn bias.
Seventeen turned left and 21 turned right (2=0.237,
P=0.626) in one group, and 16 turned into the left arm and 19 turned
right in the other treatment (2=0.114, P=0.736).
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2=1.829, P=0.176). Fourteen control animals turned
left, 17 turned right (2=0.129, P=0.720).
Repeated traverses in the maze after antennal ablation
Animals with one ablated antenna were more likely to turn towards the side
of their intact antenna over the 30 days of observation (Wilcoxon rank:
Z=-2.197, P=0.028; Fig.
3A).
Ablating other appendages
Crayfish with both antennae ablated, as well as selectively ablated chelae,
turned into both maze arms. Of the control animals with both chelae intact, 23
animals turned left and 14 turned right (2=1.730,
P=0.188). In animals with one chela ablated, 23 turned away from
their intact chela, 11 turned toward it (2=3.559,
P=0.059). Of the animals with both chelae ablated, 20 turned left and
18 turned right (2=0.026, P=0.872).
Temporal aspects of exploration
The control cohort of animals walked to the junction in 21.0±29.9 s
(mean ± s.d.) and were in the junction for 7.8±4.4 s before
crossing a decision line. The travel time of crayfish in the four experiments
was not influenced by the injuries (P>0.05; Figs
3B,
4). In the repeated traverse
experiment (no. 3), the time in which crayfish walked to the start of the
junction was different across the 30-day testing period but this was for both
treatments (P=0.049; Fig.
3B).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). When part of one antenna was removed, C. destructor did not display a turn bias toward the intact side. This suggests that a reduced level of information is sufficient for normal exploratory behaviour. In these trials, the percentage of crayfish that turned toward the intact side was similar to that observed in the base ablated animals. This suggests there may be a threshold of tactile information required for normal exploratory behaviour and that our partial ablation placed the animals close to that point.
There is some evidence that varying the sensory input also influences
temporal aspects of crayfish exploration. Walking speed in a maze is increased
by the selective removal of antennal input
(McMahon et al., 2005). On the
other hand, there is also evidence that the selective removal of chemical
input from antennules results in slower locomotion
(Kraus-Epley and Moore, 2002).
The results of this study fall somewhere between these two outcomes. Walking
speed was the same for all treatment groups within each experiment. It may be
that the large variation in walking speed of the animals in this study
prevented the detection of differences.
Does experience compensate for lost antennae?
Antennal damage affected behavioural outputs of C. destructor but
prior knowledge also affected the outcome. If the antennal ablation occurred
prior to exploring the area, the animal's search strategy was affected,
whereas if the crayfish had previously explored the environment with intact
appendages, subsequent injury did not affect turn behaviour. This agrees with
studies that indicate sensory input available at the time new environments are
encountered influences behaviour (Basil and
Sandeman, 2000; Patullo and
Macmillan, 2006). This would therefore also affect learning
processes. C. destructor and other species of crayfish can learn the
topography of an environment (Basil and
Sandeman, 2000; Shuranova et
al., 2005). This is also inferred from our results where crayfish
generally walked faster to the junction after the first two trials (experiment
3; Fig. 3). In the maze
environment, however, learning does not appear to affect turning behaviour of
intact individuals (McMahon et al.,
2005). Injured crayfish with repeated exposure to the same
environment in our experiments turned in a biased manner. Together, these
results suggest that some learning does occur in this situation and that this
was affected by antennal injuries.
In a wild environment, narrow and open spaces exist depending on how debris
and substrate are positioned. When crayfish with ablated antennae walk around
a larger, more open arena than the maze in this study, they do not
dishabituate to the environment as they do when the antennae are intact
(Basil and Sandeman, 2000).
This indicates that learning is inhibited in wider spaces. We observed a
behavioural change in animals placed in the narrow maze with no prior
experience. This suggests that crayfish may process tactile information from
open and confined areas in a similar manner. We could therefore predict the
same result as in our narrow maze in a familiar open arena. That is, animals
that previously explored in an open environment without injury, would not
change behaviour in a subsequent trial with a restrained or injured
antenna.
Can other appendages and receptors be used to compensate for lost antennal information?
The chelae manipulations did not result in biased turning behaviour. If
these appendages functioned as tactile receptors to replace lost antennal
information, one would have predicted a change in turn behaviour when one
cheliped was ablated. It is known that tactile receptor setae are located on
the chelae (Tazaki and Ohnishi,
1974; Solon and Kass-Simon,
1981), so it is interesting that the bilateral ablations produced
no result. This may have occurred because the chelae are closer to the
carapace than the antennae so they have a smaller range to detect objects and
would probably do so after the antennae in most instances. Therefore, even if
they use a bilateral comparison method similar to that thought to be used by
the antennae and antennules (McMahon et
al., 2005), they would provide a less valuable system for
assessing directional tactile cues. Although we concentrated our focus on a
compensatory function, this suggests that the tactile systems of chelae
operate in a different manner, or perhaps for different purposes, from the
antennal tactile system. Behaviours such as the defence response
(Glantz, 1974;
Kelly and Chapple, 1990),
which also involve the chelae, might be more strongly affected than
exploration if chelae were injured.
There are some other observations of chelae use during exploration. When
the antennae are immobilised, the dactyls touch walls, particularly when
crayfish arrive at the corners of a large arena and the animals do not walk
near the walls (Basil and Sandeman,
2000). Together with our results, this suggests that the chelae
are not used to direct movement when the antennae otherwise would. In a
larger, more open arena than our maze, slower velocities have also been
recorded for C. destructor when the antennae are restrained
(Basil and Sandeman, 2000).
Although we did not measure velocity per se, it seems that we did not make
that observation here because travel times to, and through, the junction were
similar to the control cohort. Injured C. destructor may therefore be
able to learn terrain, or use other tactile input (i.e. from the legs) to
contribute to path integration in narrow spaces in lieu of antennal tactile
information.
Compensation for injury is possible in some arthropod species. For example,
if the crab Calinectes sapidus loses only one cheliped, and the
spider Pardose milvina loses only one or two legs, measured
behaviours do not differ from those of intact individuals
(Brautigam and Persons, 2003;
Smith and Hines, 1991).
Individuals do, however, become significantly disadvantaged if further limb
loss occurs. In some instances it has been highlighted that compensation can
occur but this is insufficient to overcome the injury
(Brock and Smith, 1998). Our
study indicates that the tactile system of C. destructor can overcome
minor injuries, such as partial antenna loss, but major damage, such as
complete antenna loss, modifies behaviour.
Implications for tactile systems
Tactile systems used by arthropods to explore terrain vary in
sophistication. Examples from several taxa describe several functions
including following walls and surfaces as well as distinguishing between
different textures [e.g. ants (Dussutour
et al., 2005), cockroaches
(Camhi and Johnson, 1999),
crayfish (Patullo and Macmillan,
2006)]. Touch is probably important in other behaviours that
require the body to be orientated in a particular way. One example is when
aquatic decapods navigate or search in odour plumes. The process is largely
governed by chemical cues (e.g. Reeder and
Ache, 1980; Weissburg and
Zimmerfaust, 1994; Kozlowski
et al., 2003) but studies also suggest that a number of sensory
inputs, such as vibration, could provide additional information
(Weissburg and Zimmerfaust,
1994; Finelli et al.,
1999; Horner et al.,
2004). Decapods can navigate by magnetic fields [Panulirus
argus (Lohmann et al.,
1995)], orientate toward swimming and stationary prey items
[C. destructor (Zeil et al.,
1985), P. clarkii
(Breithaupt et al., 1995)] and
rear into defence postures [Cambarus bartonii
(Kelly and Chapple, 1990)].
These are other possible behavioural situations that could combine tactile
information with other cues.
Some issues about crayfish tactile exploration remain unclear. For example, whether the effects of antennal removal persist until moult, and therefore regeneration, is unknown. An experiment in which treatments consist of ablations at a set period before trial, with no animals trialled twice, may be appropriate to remove inherent experience effects. Behavioural outcomes are likely to be affected by the modalities in play, but how information from supplementary sources is integrated with tactile information is not fully resolved. For example, the way vision affects tactile exploration, and understanding how different modalities work together is important for understanding haptic systems of crustaceans and other taxa.
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Acknowledgments |
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