Chem. Senses 27: 49-55,
2002
© Oxford University Press 2002
Bilateral and Unilateral Antennal Lesions Alter Orientation Abilities of the Crayfish, Orconectes rusticus
J.P. Scott Center for Neuroscience, Mind and Behavior, Laboratory for Sensory Ecology and Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, USA
Correspondence to be sent to: Paul A. Moore, Laboratory for Sensory Ecology, Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403-0212, USA. e-mail: pmoore{at}bgnet.bgsu.edu
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Abstract |
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Numerous animals use chemical cues within their environments to execute various behaviors. One of these behaviors is orientation to an odor source. Crayfish, in particular, can orient to food sources under a number of different conditions. It has not been determined, however, what kind of search strategy these animals employ to successfully locate a food source. To determine the role of antennae and antennules in this behavior and to investigate different modes of orientation behavior, the orientation patterns of crayfish with complete and partial antennal lesions were examined. Detailed analysis of orientation paths confirmed that crayfish could not locate odor sources with either bilateral or unilateral lesions. This suggests that crayfish are using the spatial information obtained from these appendages to successfully orient. Animals using information from the bilaterally paired appendages in the control group exhibited increased walking speed, increased speed to source and decreased heading angles towards the source compared to these measurements taken from lesioned groups. There was no significant difference in any parameters between animals with unilateral or bilateral lesions. This strongly suggests that these animals are reliant on the spatial comparison of differences between bilaterally paired olfactory appendages for successful orientation.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Studies focusing on chemical orientation through olfactory cues, especially in aquatic organisms, have proliferated in recent years in an attempt to understand orientation strategies (McLeese, 1973
;
Reeder and Ache, 1980;
Moore et al., 1991;
Breithaupt et al.,
1999; Moore and Grills,
1999; Finelli et al.,
2000; Weissburg,
2000). Different organisms have been found to employ various
orientation strategies when presented with chemical stimuli. The two main
types of orientation mechanisms that have been explored in detail differ only
in the degree by which spatial decisions are controlled by the chemical
stimuli. These are odor-modulated optomotor anemotaxis (terrestrial) and
odor-gated rheotaxis (aquatic) versus chemotaxis.
Moths have been found to use odor-modulated optomotor anemotaxis (Vickers
and Baker, 1992,
1994; Mafra-Neto and
Cardé,
1994,
1995). During orientation, the
moth switches between a casting behavior and an upwind surge in the presence
of odor. The duration of the surge is controlled by the frequency with which
odor filaments contact the receptors on the antennae. Blue crabs use
odor-gated rheotaxis in orientation
(Weissburg and Zimmer-Faust,
1993). While orienting, the crabs use both the direction of flow
and the intermittency of the chemical signal to find the odor source. Crayfish
and lobsters, which orient using chemotaxis, extract directional information
directly from the odor plume, which is used in orientation
(Moore et al., 1991;
Atema, 1996;
Moore and Grills, 1999). It
has been determined that the animal remains in the center of the odor plume
and moves towards the source by the use of spatial and temporal comparisons.
Moore et al. (Moore et
al., 1991) classified the search patterns of lobsters in odor
plumes into three distinct search phases. The phases are as follows: the
initial stage is marked by increased walking speeds and decreased heading
angles, the intermediate stage is identified by constant walking speeds and
headings and the final stage consists of decreased walking speeds and
increased heading angles. Up to now the strategy used by crayfish during
chemical orientation has remained unknown. Detailed descriptions of these and
other orientation mechanisms can be found elsewhere
(Bell and
Cardé, 1984;
Kennedy, 1986).
Although there has been much debate about defining specific terms related
to various modes of orientation, it is widely recognized that organisms use
different mechanisms to orient to a point source. These mechanisms can be
classified as either a taxis or kinesis
(Van Der Steen and Ter Maat,
1979). Orientation responses during a taxis, such as turn angles
and heading angles, are directly guided by the spatial distribution of the
stimulus (Fraenkel and Gunn,
1961; Bell and
Cardé, 1984). Typically, this is
performed through information obtained from spatially separated receptors.
Orientation through odor-modulated optomotor anemotaxis and odor-gated
rheotaxis is dependent not only on the structure of the odor plume, but also
on the flow direction of the medium and the visual flow field. Therefore, both
mechanoceptors, chemoreceptors and visual receptors are necessary to
successfully orient using these search strategies. During a kinesis,
orientation responses, such as turning rate and walking speed, are not made
with respect to the direction of the stimulus, but involve a change in the
rate of behavior being performed by an organism
(Fraenkel and Gunn, 1961;
Bell and
Cardé, 1984;
Schöne,
1984). Kinesis is performed by comparing information in a temporal
fashion. Spatially separated sensory appendages are not necessary to
successfully perform a kinesis.
Dunham et al. (Dunham et
al., 1997) found, through ablation, that antennules are not
necessary for detection of sucrose in the crayfish Cambarus bartonii.
However, the antennules were found to be necessary for substrate searching
during orientation and also for leg-to-mouth feeding. Also, Giri and Dunham
(Giri and Dunham, 2000)
collected data supporting the hypothesis that antennules are necessary for
orientation to an odor source. They found that the total ablate groups in the
study initiated search behavior at a much closer distance to the source than
the partial ablates and intact animals. Several studies focusing on the
lesioning of olfactory organs have shown that unilateral ablation of lobster
lateral filaments resulted in the loss of directional choice ability while
unilateral medial lesioning had no effect
(Devine and Atema, 1982).
Belgane et al. (Belgane et
al., 1997) found that lobsters must have both antennules to
orient in the far field. Crayfish were the ideal organisms for the present
study due to the fact that they respond to chemical stimuli present in their
environment (Hazlett, 1985a,
b) and forage on patchily
distributed food sources.
The present study attempted to interpret whether or not full or partial lesioning of crayfish antennae and medial and lateral filaments affected chemical orientation to a food source. It has not been determined if lesioned crayfish, both bilaterally and unilaterally lesioned, are capable of locating a food source. With this in mind, if crayfish were using taxis, it would be expected that individuals with both antennae lesioned would not be receiving chemical or mechanical stimulation at either antenna and, therefore, would not exhibit a search behavior. Animals with a unilateral lesion will receive mechanical and chemical stimulation on one side only. It would be expected that these animals would be unable to successfully locate the odor source due to the fact that there is no spatial separation between unlesioned receptors, a condition necessary for taxis. This study sought to determine what mechanism is used to successfully orient, namely to differentiate between the use of kinesis or taxis.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Animals
The crayfish (Orconectes rusticus) used in this study were from the Portage River near Bowling Green State University in Bowling Green, Ohio. The animal carapace lengths were measured and only intermolt males (3.3-32.0 g) with intact appendages were used (i.e. antennae, lateral and medial filaments, chelae and walking legs). Animals were considered to be intermolt if they did not molt for 2-3 weeks after experimentation. All animals were stored in individual containers with a diameter of 16 cm and a depth of 9 cm. Animals were visually and mechanically isolated for a minimum of 72 h in a recirculating housing tank on a light cycle of 14 h light: 10 h dark before use. The animals were fed one pellet of dried rabbit food three times per week.
Stimulus
The stimulus for all trials consisted of a block of fish gelatin (average 9.0 ± 0.78 g, average 2.5 ± 0.20 x 2.5 ± 0.13 cm). Fish gelatin was made by homogenizing cod (average 47 ± 1.6 g) and 235 ml of cold water. Four packets of Knox unflavored gelatin were mixed with 471 ml of hot water, which was then mixed with the fish homogenate. The mixture was poured into a rectangular pan, covered with plastic and refrigerated until solid. The gelatin was cut and each cube was individually wrapped in plastic and refrigerated until time of use.
Flume
All trials were conducted in a 760 l recirculating flume (complete dimensions, 200 x 62 x 52 cm; working section, 104 x 53 x 27 cm). The flume was constructed using clear plexiglas sheets for the sides of the chamber and the frame was constructed of wood beams. Two sheets of fluorescent light grating (egg crates, 169 mm2 holes) wrapped with plastic screen (1 mm2 holes) were placed upstream and one placed downstream to serve as collimators. Average flow velocity (3.63 ± 0.16 cm/s) was measured in the middle of the flume with a Marsh-McBirney Model 2000 Portable Flow Meter. The air-powered motor (Eclipse Systems, model no. 9-4300-14A) was allowed to run for at least 1 h before the first acclimation period. A maximum of three trials were run each time the flume was filled.
The bottom of the flume was lined with a thin layer of gravel (
5-8
mm). A shelter (6 x 12 cm) was constructed from a PVC pipe cut in half
lengthwise. This shelter was used to acclimate the animal to the tank and was
placed at the downstream end of the working section on the middle of the back
wall. The bottom of the shelter was enclosed in a wire screen and the
downstream end was enclosed in plastic grating. A weighted, removable plastic
grate was placed at the upstream end to completely enclose the shelter.
The food source was placed directly on the substrate upstream of the animal. The exact position of the gelatin was 71.36 cm upstream from the downstream collimator of the flume.
The exterior walls of the flume were covered with black material so as not to disturb the animals with outside activity. A video camera (Panasonic Color CCTV camera, model no. WV-C1350) was mounted above the flume. Trials were recorded on a Panasonic VHS recorder (model no. AG-1970). All orientation trials were performed between 08:00 and 17:00 hours.
Lesion protocols
The treatment groups consisted of the following: (i) no treatment or control (herein called control); (ii) both antennae and antennules lesioned (herein called both); (iii) right antenna and antennule lesioned (herein called right); (iv) left antenna and antennule lesioned (herein called left). Twelve individuals were used in each of the four experimental groups. Experimental animals were placed on ice for 10 min before being placed in restraints and glued with Kwik-Fix brand superglue. Animals were put on ice to further slow their movements while in the restraints. The glue was applied using the applicator tip of the glue tube. Glue was applied to the antennae and antennules of experimental animals beginning at the base and extending to the tip and covering the aesthetasc hairs. Controls were put on ice for 10 min and a similar amount of glue was placed at the base of the carapace to ensure that behavior was not affected by the smell of the glue. Antennae and antennules of controls were washed with flume water using a syringe. This was done to simulate physical stimulation of the antennae and antennules of experimental individuals during gluing. Extreme care was taken to avoid getting glue on any anatomical parts other than the antennae and antennules. The glue was completely dry before the individual was placed in the holding container for temperature acclimation.
Testing methods
Before being placed in the flume, crayfish were acclimated to the temperature change from the holding tank (average 24.5 ± 0.29°C) to the flume (average 21.3 ± 0.41°C) for a minimum of 20 min in a holding container with flume water.
After gluing and temperature acclimation, the individual was placed at the downstream end of the flume in the shelter. Animals were allowed to acclimate to the flow for 19 min before the start of the trial. The gelatin was removed from the refrigerator at the beginning of each acclimation so it would be at room temperature for the trial. Each animal was exposed to the odor source for 1 min before video taping began and the start gate of the shelter removed. A trial was terminated when the animal found the food source or if the animal did not locate the odor source within 10 min. A successful trial was one in which the animal physically contacted the food source. A new piece of gelatin was used for each trial.
Analysis
A Peak Motus Motion Analysis System was used to digitize the taped trials.
For each trial the tip of the rostrum was digitized at 1 point/s. The rostrum
was digitized because these animals can walk sideways and backwards. We were
not concerned with body orientation but with the overall movement of the body.
These parameters were chosen based on Moore and Grills
(Moore and Grills, 1999). Many
lesioned animals spent the entire 10 min walking around the tank. For all
animals that located the source the whole orientation path was included in the
analysis. The trials of animals that did not successfully locate the odor
source were cropped to the average time of control trials. Since some
orientation parameters, namely walking speed and speed to source, are
sensitive to total time spent orienting, we only analyzed the first 70 s of
experimental trials. This time period was chosen because it was the average
orientation time of control trials. We analyzed the following orientation
parameters: percent success of finding the source, distance from the source
(cm), speed to the source (cm/s), walking speed (cm/s), heading angle towards
the source, net to gross ratio or straightness of path, heading angle upstream
and turning angle towards the source
[Figure 1, taken from
(Moore et al.,
1991)]. A MANOVA was performed to detect differences between
groups for each parameter, followed by a post hoc comparison of LSD
with a P value of <0.05. The success rate of each group in
locating the source was analyzed using a 
2 statistic. We then
used the
Dunn—
idák
method to correct for multiple comparisons. The new P value used to
determine significance was P < 0.013.
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) at point t =
0 is calculated. Line B represents the straight line to the odor source
(asterisk) from which a heading angle relative to the odor source (ß) is
calculated. Line D represents a path that is straight upstream, from which a
heading angle relative to upstream ( |
Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Qualitative description of orientation
Orientation paths were qualitatively different between control and experimental groups (Figure 2). Control individuals (no treatment) were clearly attracted to the fish gelatin, whereas experimental individuals showed no stereotyped paths. Orientation paths were visibly different between the four treatment groups.
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The success rate of finding the source was markedly different between
groups. All lesions had significant effects. Significance was found between
the control group and each of the experimental groups
(Figure 3A). Numbers of animals
finding the source were as follows: 9 of 12 controls located the source, 1 of
12 individuals with bilateral lesions found the source, 1 of 12 individuals
with the right lesion located the source and 0 of 12 individuals with the left
lesion located the source. Statistical differences were as follows: control
group and both (2 = 69.8, n = 12, P <
0.001); control group and right (2 = 68.8, n = 12,
P < 0.001); control group and left (2 = 6.75,
n = 12, P < 0.01).
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Effects of impairment on walking
Antennal impairment was also found to affect walking speed. Significant differences were noted between control individuals and all treatment groups with respect to the average speed to the source (Figure 3B). Lesioned animals had slower walking speeds towards the source. Significant differences were found between the control group and each of the experimental groups. Statistical differences were as follows: control group and both (n = 12, P < 0.0001); control group and right (n = 12, P < 0.002); control group and left (n = 12, P < 0.0003). Lesioned animals were also found to walk more slowly in the presence of odor (Figure 3C). The control group was found to be significantly different from both (n = 12, P < 0.003) and right (n = 12, P < 0.02). Significance was also found between both and left (n = 12, P < 0.05).
Treatment effects on orientation
Lesioned animals were found to have significantly greater heading angles (Figure 3D). This indicates that a less direct path was taken to the odor source by lesioned animals. Significance was found between the control group and each of the experimental groups: control group and both (n = 12, P < 0.02); control group and right (n = 12, P < 0.03); control group and left (n = 12, P < 0.004).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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While antennae and antennule sensory input are necessary for successful orientation to a food source, it is the bilateral information received though these appendages that is a crucial element of this behavior in crayfish. Lesioned crayfish rarely located the odor source, had much slower walking speeds and greater heading angles. This suggests that impairment of bilateral information from chemoreceptors and mechanoreceptors significantly affects the ability of crayfish to orient to odor sources. Since there is no significant difference between unilaterally and bilaterally lesioned groups, this indicates that spatial information is critical to orientation behavior.
This finding complements that for lobsters found by Belgane et al.
(Belgane et al.,
1997), that orientation by lobsters was impaired by the loss of an
entire antennule but was not affected by the loss of only the chemoreceptors
on one antennule. The lesioning technique used by Belgane et al.
consisted of dipping the antennule in deionized water for 5 min, resulting in
the lysing of chemoreceptor dendrites while the mechanoreceptors remained
intact. By using glue to lesion the animals in the current study, not only the
chemoreceptors but also the mechanoreceptors were blocked. Our findings also
support the conclusions of Webster et al.
(Webster et al.,
2000) that spatial information is important to and, in fact, is
used during orientation.
Upon analysis of the results, the data suggest that crayfish are using
taxis and not kinesis in orientation. Because we lesioned both chemo- and
mechanoreceptors on the antennae and antennules, it is difficult to say how
much of a role perception of flow direction plays in orientation. Our results
clearly show that with a deficit of spatial information it is difficult for
these animals to orient towards an odor source. Weissburg
(Weissburg, 1997) states that
although the term `chemotaxis' has been used to describe orientation in
turbulent plumes, it is unlikely that this behavior is a strict taxis (i.e. a
behavior guided by a concentration gradient). This is because smooth
concentration gradients cannot persist in turbulent waters. Blue crabs use
odor-gated rheotaxis, or the directionality of flow patterns and the
intermittency of the chemical signal, to orient to odor sources
(Weissburg and Zimmer-Faust,
1993). It is thought that the animal measures the angle at which
it exited the odor plume and re-enters the plume at the exact same angle.
Therefore, blue crabs find the odor source by following the edges of the odor
plume. In odor-modulated optomotor anemotaxis, as seen in moths, the animal
switches from a casting behavior to an upwind surge in the presence of an odor
signal (Vickers and Baker,
1992,
1994; Mafra-Neto and
Cardé,
1994,
1995). The duration of this
behavior is controlled by the frequency with which odor filaments contact the
antennae. Finally, it appears that lobsters extract detailed information from
the odor plume which provides directional information to the animal during
orientation (Moore et al.,
1991; Atema, 1996).
Spatial and temporal comparisons of information within the plume allow the
lobster to find the center of the plume and move towards the odor source.
If crayfish used a kinesis type of orientation, we would expect to find significant differences between the treatments with both appendages lesioned and those with a unilateral lesion and no differences between controls and those with unilateral lesions. In kinesis, even with unilateral lesions, the animals would still have the capability to extract temporal information from the odor plume and successfully orient. We suggest that the animals with one intact antenna are attempting to orient using the unilateral signal they are receiving. Because the animal cannot interpret the spatial characteristics of the odor plume with only one antenna, the individual will follow the signal it is receiving until it has exited the odor plume and no longer receives the signal. The individual then engages in non-directed search behavior.
The results of our study also suggest that other sensory appendages, such
as walking legs and mouthparts, do not play a primary role in orientation. We
can conclude that the antennules and/or antennae are necessary for orientation
and that orientation cannot occur with information from the walking legs and
mouthparts only. From an ablation study using the crayfish Procambarus
clarkii, Giri and Dunham (Giri and
Dunham, 1999) suggested that information being received though the
antennules is necessary for long-distance orientation but not for orientation
over short distances and that the lateral filaments are most likely the
primary olfactory organ. Although these findings appear to relate to the
findings of the present study, it is difficult to determine the true relevance
of the study by Giri and Dunham due to a lack of experimental information.
This is contrary to how intact lobsters have been found to behave during a
local food search (Moore et al.,
1991). It has been determined that the walking legs of lobsters
play a role in extracting spatial information during chemical orientation
(Devine and Atema, 1982).
Animals in this study showed preferential turning towards the intact side only
when chemoreceptors on the walking legs of the lobsters were also lesioned
using glue. This suggests that in lobsters the receptors on the walking legs
play a secondary role in spatial orientation. It was also determined that leg
receptor input was not necessary for successful orientation if the antennules
were left intact.
These results give us insights into the behavioral orientation of an impaired animal in its natural environment. Animals with full or even partial impairment will not be able to successfully orient from long distances to food sources or any other chemical sources of interest, such as mates or predators.
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Acknowledgments |
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We thank the Laboratory for Sensory Ecology and the Crayfish Journal Club at Bowling Green State University for their help in revising the manuscript. This work was funded by NSF grant IBN-9514492.
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Accepted September 18, 2001
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