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First published online December 26, 2008
Journal of Experimental Biology 212, 313-324 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022459
The cardiac response of the crab Chasmagnathus granulatus as an index of sensory perception
Laboratorio de Neurobiología de la Memoria, Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IFIBYNE-CONICET, Buenos Aires 1428, Argentina
* Author for correspondence (e-mail: ghermitte{at}fbmc.fcen.uba.ar)
Accepted 27 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: invertebrates, cardiac response, behavior, sensory perception
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
In decapod crustaceans many studies have used the changes in a vegetative
index to monitor the effects of a wide range of environmental variables on the
physiology: water currents (Larimer,
1964), PO2
(Airriess and McMahon, 1994),
ammonia (NH3) (Bloxham et al.,
1999), heavy metals (Aagaard et
al., 2000), ambient CO2/O2
(Gannon and Henry, 2004),
water temperature (Camacho et al.,
2006). In addition, the responses to several types of stimuli
(tactile and chemical cues) were examined for their effects on the heart and
ventilatory rate of crayfish, finding a reflex inhibition in the majority of
them (Larimer, 1964). More
specifically, bradycardia or reversible heart arrests have been reported in
crabs, lobsters and crayfish to a variety of optical and tactile stimuli
(Cuadras, 1980;
Cumberlidge and Uglow, 1977;
Florey and Kriebel, 1974;
Grober, 1990a;
Grober, 1990b;
Larimer and Tindel, 1966;
McMahon and Wilkens, 1972;
Mislin, 1966;
Shuranova and Burmistrov,
2002; Uglow, 1973;
Wilkens et al., 1974).
Furthermore, another set of results also gathered in crustacea have shown that
even though no observable behavioral responses were elicited, heart rate was
measurably affected by small disturbances in the environment or by social
interaction (Li et al., 2000;
Listerman et al., 2000;
Schapker et al., 2002). Given
the remarkable sensitivity of this parameter to a variety of sensory
modalities it has been posed that the cardiac response can serve as an
indicator of perception in decapod crustaceans and could well be utilized in
studies on perceptual physiology.
Our interest in altering the illumination stemmed from earlier studies
which revealed that white light causes cave crayfish to seek shelter
(Li and Cooper, 1999), and
others which showed (Grober,
1990b; Li et al.,
2000; Schapker et al.,
2002) that light (infrared, dim red, and white) can induce
alterations in crayfish's heart rate.
Both antennae of crustacea bear sensory flagella which carry
mechanoreceptive sensilla (Derby,
1982) enabling them to use tactile and mechanical cues to extract
information from the environment (Patullo
and Macmillan, 2005). These cues enable animals to find resources,
orient to water currents or escape predators
(Weissburg, 1997). In
addition, mechanoreceptive neurons responsive to stimulation have been found
all over crabs, lobsters and crayfish
(Arechiga et al., 1975). Thus,
we planned to assess a mechanosensory cue, i.e. an air puff, by looking for
changes in heart rate.
Visual cues, such as natural and artificial objects, including
two-dimensional shapes, can influence or guide directional orientation of
decapod crustaceans in specific situations
(Chiussi and Diaz, 2002;
Cuadras, 1980;
Diaz et al., 1994;
Diaz et al., 1995a;
Diaz et al., 1995b;
Herrnkind, 1983;
Langdon and Herrnkind, 1985;
Orihuela et al., 1992).
Furthermore, our own work in Chasmagnathus shows that upon the sudden
presentation of a rectangular screen passing above the animal, the visual
danger stimulus (VDS), the crab responds with a running reaction in an attempt
to escape (Maldonado, 2002),
while a cardiac response is also elicited by the same stimulus
(Hermitte and Maldonado,
2006). Consequently, the effect of presenting a VDS as a visual
cue was further explored.
Finally, the ability to detect and react to looming objects is present in
most visual animals from insects to mammals even though their visual systems
are largely different. Behavioral reactions elicited by looming stimuli have
been studied in taxa as diverse as insects, amphibians, birds, and mammals
(Jablonski and Strausfeld,
2000; Maier et al.,
2004; Regan and Hamstra,
1993; Tammero and Dickinson,
2002; Yamamoto et al.,
2003). Taking into account that in the crab Chasmagnathus
a robust and reliable escape response can be elicited by computer-generated
looming stimuli (Oliva et al.,
2007), we decided to explore the possibility that virtual
collision stimulus might elicit physiological responses as well.
Therefore, our working hypothesis is that a physiological parameter such as
heart rate can constitute a sensitive index to assess crustacean perceptual
capacity. The purpose of our study was to examine stimuli characterized as
innocuous (a light pulse and an air puff) and those regarded as threatening (a
visual danger stimulus and virtual looming stimuli), comparing their effect on
both cardiac and locomotor activity. In addition, both escape and cardiac
response latencies to looming stimuli were simultaneously recorded with the
purpose of comparing them and examining the relationship between them. Similar
to vertebrates, invertebrates may also need rapid cardiovascular and
respiratory regulation to be primed for `fear, fight or flight' when the need
arises (Wilkens and McMahon,
1992). The ability to escape predation or to be alerted to subtle
changes in the environment in relation to autonomic control is associated with
the complex ability to integrate sensory information as well as motor output
to target tissues. Very few previous studies have investigated the
simultaneous occurrence of autonomic and somatic responses in invertebrates
(Hermitte and Maldonado,
2006). Thus, a broader objective was to further investigate how
these more integrated strategies work in invertebrates.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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, at a pH of 7.4–7.6, and
maintained within a range of 22–24°C. The holding and experimental
rooms were maintained on a 12 h light:dark cycle (lights on 7:00 h to 19:00 h
and 22–24°C. Experiments were run between 8:00 h and 19:00 h and
performed within the first two weeks after the animals' arrival. Each crab was
used only in one experiment. All the recording experiments were conducted 2 or
3 days after the initial wiring of the animals (see below). During this
recovery period, crabs were kept in individual tanks and fed rabbit food
pellets (Nutrients, Argentina) daily. Following tests, animals were returned
to the field and released in an area 30 km away from the capture area.
Experimental procedures were in compliance with the Argentine laws for Care
and Use of Laboratory Animals. Both unrestrained and restrained animals were used in different experiments. The restrained condition was achieved by immobilizing crabs prior to the experiment enclosing them in close-fitting thick elastic bands, with the legs positioned in an anterior position and slightly under their bodies to restrict movement. This procedure allowed us to stabilize the electrocardiogram (ECG) making the quantification of heart rate easier.
Cardiac response: recording procedure
A small jack was cemented with instant adhesive to the dorsal carapace in a
position anterior to the heart and had two metallic pins where the electrodes
were soldered. These were made of silver wire (diameter 0.25 mm, VEGA &
CAMJI S.A., Argentina) cut in sections 2.4 cm long. The free end of both wires
was inserted in holes previously drilled in the cardiac region of the dorsal
carapace placed to span the heart in a rostral–caudal arrangement and
separated by 4–5 mm. The electrodes easily pierced the hypodermis and
were cemented in place with instant adhesive
(Fig. 1). All the recording
experiments were conducted 2–3 days after the initial wiring of the
animals in order to allow them to recover from the stressful handling because
it has been shown that it alters heart rate (HR) for a few days
(Wilkens et al., 1985;
Listerman et al., 2000). Prior
to an experiment, the crab was lodged in the container called an actometer: a
bowl-shaped opaque container with a steep concave wall 12 cm high (23 cm top
diameter and 9 cm floor diameter) covered to a depth of 0.5 cm with sea water
and illuminated with a 10 W lamp placed 30 cm above the animal. A plug
connected to the impedance converter (UFI, model 2991, California, USA) was
slotted in each jack cemented on the animal in order to monitor HR. The
impedance converter measures the changes in the resistance between two
electrodes, associated with the hemolymph movement after each heart
contraction (Li et al., 2000;
Listerman et al., 2000;
Schapker et al., 2002). The
output from the impedance leads was sent to the analog-to-digital converter of
a computer data acquisition and analysis system
(Fig. 2Ai).
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Environmental disturbances
To test the crabs' perception of particular environmental alteration, the
study was divided into four experimental conditions according to the different
stimuli used in each one: (1) a 2 s white light pulse; (2) either a 3 s or 5 s
air puff; (3) the projection of four different computer generated looming
stimuli on a flat screen and (4) a moving visual danger stimulus (the VDS).
Between 11 and 17 crabs were tested in each experimental condition. Both
cardiac and locomotor activity could be simultaneously recorded. Unrestrained
and restrained animals were used.
The light pulse stimulus
A 2 s pulse from a white-light-emitting diode (LED) was presented 7 cm from
above the animal (Fig. 2Ai).
The specification for a 5 mm white LED is: luminous intensity 10,000 mcd;
viewing angle: 23°. The illumination intensity measured in the actometer
was 450,06 mW m–2 and 1.266,66 mW m–2 before
and after stimulation, respectively.
The mechanosensory stimulus
An air puff was generated by an air pump and delivered through a thin
plastic transparent tube directed towards the animal and positioned 1 cm above
the cephalothorax carapace (Fig.
2Ai). Stimulus duration could be precisely controlled, lasting
either 3 or 5 s. Every animal in this experimental condition was tested with
both stimuli, with a 3 min interval between them and varying the order in
which the stimuli were presented to each animal.
The looming stimulus
Computer-generated visual stimuli were projected on a flat screen monitor
(Phillips 107T, horizontal and vertical screen dimensions 32x24 cm,
respectively, refreshing rate 60 Hz), located 20 cm in front of the animal
(Fig. 2B). ECG and/or locomotor
activity records began after a black curtain was lowered in the front part of
the cage and after the animal had remained visually undisturbed for 10 min.
The illumination intensity measured in the setup was 250±5 mW
m–2 and 53±5 mW m–2, before and after
the expansion, respectively. All visual stimuli were generated from a single
PC using commercial software (Presentation 5.3, Neurobehavioral Systems Inc.,
USA). Visual simulations generated by computer may differ in many ways from
the visual input experienced under natural conditions. Nevertheless, no escape
response differences were found in Chasmagnathus when comparing a
black sheet of cardboard moving overhead with the computer-generated image (V.
Medan and D. Tomsic, personal communication). The simulated looming stimulus
used in the present study consisted of a 5 cm black square, which approached
over a distance of 70 cm at different constant speeds of 5, 10, 20 and 40 cm
s–1, generating a different angular size for the virtual
approaching stimulus as a function of time
(Oliva et al., 2007).
Throughout the experiments, expansions were always directed towards the animal
(see Fig. 2C). Every animal in
this experimental condition was tested with the four looming stimuli, with a 3
min interval between them and counterbalancing the order in which the stimuli
were presented to each animal.
The visual danger stimulus
An opaque rectangular screen (25 cmx7.5 cm), i.e. the visual danger
stimulus (VDS), positioned 6 cm above the container, was moved horizontally
from left to right and vice versa (Fig.
2Ai). A VDS lasted 5 s and consisted of two successive cycles of
screen movement (Fig.
2Aii).
Data analysis
The cardiac activity was recorded during an interval of 9, 10 or 20 s,
during which the stimulus was presented after a 3 s delay. The duration of the
cardiac event or period was measured and used to calculate the instant heart
rate (IHR) as the inverse of the period (IHR=1/p). A number of
previous studies in crustaceans have shown that heart rate can vary widely
both between and within individuals and with the experimental conditions
(Grober, 1990a;
Hermitte and Maldonado, 2006).
For this reason we normalized the IHR (normalized
IHRi=IHRi/IHRM; where IHRi is the
IHR of each single event and IHRM is the mean IHR). To control that
changes in the IHR due to the stimuli were significantly different from
spontaneous changes in the IHR, two ratios (R1 and
R2) were statistically compared
(Fig. 2D).
R1 represents the quotient between IHR1 (the
IHR of one event randomly selected prior to stimulus on-set) and the
IHRM (R1=IHR1/IHRM).
R2 represents the quotient between the IHR2
(the IHR of one representative event during the cardiac response) and the
IHRM (R2=IHR2/IHRM).
Since changes in heart rate in response to sensory stimulation are usually
rapid and very brief (Grober,
1990a), the 9, 10 or 20 s recording time provided a suitable
interval for measuring cardiac responsiveness to sensory stimulation.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The relationship between escape and cardiac responses
Fig. 4 shows a
representative example of two different animals whose heart rate and locomotor
activities (LA) were simultaneously recorded. When no stimulus was presented,
spontaneous walking activity was observed while no heart arrests were
identified, revealing the independence of each pattern of activity in both
animals (Fig. 4Ai,Bi). By
contrast, upon the presentation of a different stimulus to each animal
(Fig. 4Aii,Bii), a diverse
pattern of activity could be observed. During the presentation of a seemingly
innocuous stimulus such as an air puff, it was possible to record a small but
clear cardiac response while no escape was elicited. Upon a looming stimulus
presentation strong cardiac and escape responses were concurrently
triggered.
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Upon the presentation of a 5 s air puff to restrained and unrestrained animals, a noticeable and consistent cardiac response could be observed as a decrease in the mean IHR curve immediately after stimulus started in both groups of animals (Fig. 5). A smaller but visible decrease in the IHR was also observed when the air puff ended. The restrained animals exhibited a more conspicuous response than the unrestrained animals. When a statistical analysis was performed to compare the IHR previous (R1) and during stimulation (R2), significant differences were found between them (P<0.01), revealing the sensitivity of this parameter to an air puff in the two groups (Fig. 5A,B). Together with the cardiac recording, a locomotor activity record was performed, showing no escape response to this stimulus (data not shown).
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The presentation of a light pulse could also be traced in the IHR mean curve of two other groups of crabs (restrained and unrestrained) as a small and clear response at the beginning of the stimulation and an off-response at the end, similar in magnitude to that previously detected for the air puff (Fig. 6). Once more, the restrained group displayed a larger response compared with that of unrestrained animals showing a tendency that was retained for all the stimuli used in this work. The decrease in the IHR due to the light pulse stimulation was comparable to that observed for the air puff, ranging from 10 to 15%. The statistical analysis revealed significant differences between base line (R1) and stimulation (R2) for both groups (P<0.01; Fig. 6A,B). Here again the simultaneous record of the locomotor activity could not reveal an escape response to this stimulus (data not shown).
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Two other looming stimuli were also assessed in this group of animals yielding similar results; a faster one (40 cm s–1) and one in between the previously described looming stimuli (10 cm s–1), which produced maximum responses at about 2.8 s and 6.5 s, respectively. These differences in time response can be accounted for in terms of the different expansion velocities. The statistical analysis for both stimuli revealed significant differences between base line (R1) and stimulation (R2) in restrained and unrestrained animals (P<0.01; data not shown). On the whole, the results regarding looming stimuli reveal that the IHR proved useful to estimate the perceptual capacity in these animals even when these stimuli were virtual.
From the results of these various stimulations a clear-cut conclusion can be drawn: all the stimuli tested could trigger measurable cardiac responses. In addition, from the results in Figs 7 and 8 it can be observed that the cardiac response occurred at different times for the different expansion velocities of the stimulus, showing an earlier response when the expansion was fast and a later response for intermediate and slow expansions. A similar profile was observed for the mean escape response revealing the association between both responses. This issue is discussed further in the section `Analysis of the cardiac and escape response latencies'.
Validation of the virtual looming stimulus with a real danger stimulus
In Fig. 9 the representative
normalized IHR of three different crabs during the presentation of the VDS is
shown together with the mean recording from a total of 13 animals. The bar
graph in each panel shows, for all animals, the mean IHR of one event prior to
and during a VDS presentation (R1 and
R2, respectively) revealing significant differences
between them (P<0.01) in the restrained condition. Some comments
are pertinent here: (1) this result strengthens those obtained with looming
stimuli showing comparable magnitude responses; (2) previous work with the VDS
was assessed as beats per minute (Hermitte
and Maldonado, 2006). Our present results validate those preceding
results, using a more accurate parameter, the IHR; (3) only animals in
restrained condition are shown here because the VDS elicits a strong escape
response that complicates heart rate observation in unrestrained crabs.
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The cardiac response in restrained and unrestrained animals
Some animals would not always respond to stimulus presentation, thus a
detailed analysis on response probability was performed for the whole
population previously described. Fig.
10Ai,Aii compares the probability of cardiac response to the
examined stimuli (looming stimulus, air puff, light pulse) in restrained and
unrestrained crabs. In restrained animals the response probability was always
higher than 60% and for threatening stimuli near 100%. In unrestrained animals
it was lower and the response to innocuous stimuli such as the light pulse
declined to near 30%. A frequency analysis with 
2-test for
homogeneity was performed on the pooled data of the three stimuli together
stating that the probability of response between both conditions was
significantly different
(Gyates=10.35<2(1;
0,095)=3.84).
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Analysis of the cardiac and escape response latencies
A similar profile was found for the escape and cardiac responses (Figs
7 and
8) revealing an association
between them which is worth further investigation.
Fig. 11 compares the escape
response and the cardiac response latencies to the presentation of different
looming stimuli, and shows an equivalent increase in their latencies related
to the decrease in the velocity of expansion of the stimuli
(Fig. 11A). Interestingly,
both responses showed a tight correlation (r: 0.9742;
Fig. 11B).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and investigative in nature, a strong CIR on perceiving a
threat may be considered to be part of a startle response modulated by fear
that may eventually contribute to removing the animal from the proximity of a
potentially dangerous stimulus (Laming,
1981).
Transient cardiac inhibition in vertebrates has been identified as
indicative of an emotional component by many investigators
(Davis, 1992;
Lang et al., 1972;
LeDoux, 1993) although it has
also been proposed that it may play a causal role in appropriate response
selection, and thus have adaptive significance in its own right
(McLaughlin and Powell, 1999).
The fact that cardiac inhibition has been associated with attention phenomena
(Lacey and Lacey, 1974;
Graham and Clifton, 1966;
Sokolov, 1963;
Powell, 1994) suggests that
the latter hypothesis has merit. Accordingly, it has been suggested that the
invertebrate responses to different external stimuli, which strongly depend on
the animal's functional state but less on the modality of the stimulus, appear
to be similar to those characteristic of the so-called `orienting reflex' of
higher mammals (Graham, 1979;
Pavlov, 1923;
Zernicki, 1987). Thus,
relatively `neutral' unexpected external stimuli might trigger in the
crustacean brain some processing of the information about the `novel' stimulus
and its possible consequences (Shuranova
and Burmistrov, 1996;
Shuranova et al., 2006).
However, whereas the above explanation may account for the cardiac response
to innocuous sensory stimulation, it is unlikely that it accounts for the
bradycardia observed in crabs to threatening stimuli, as this physiological
response is highly correlated with active movements away from the stimulus.
Because of the correspondence with avoidance behavior, this physiological
response may provide a useful index to determine the specific characteristics
of sensory stimuli that can elicit avoidance or startle behavior in crabs
(Grober, 1990a). Thus, the
cardiac responses of crabs to the VDS and looming stimuli may represent an
example of the so-called `startle induced bradycardia' of many animal species
to rapid and intense sensory stimuli
(Guirguis and Wilkens, 1995).
Support for this proposal comes from earlier works showing that in most cases
of intense sensory stimulation, both the heart and the scaphognathites of
decapod crustaceans exhibit a coordinated and rapid decrease in beating
(Larimer, 1964;
McMahon and Wilkens, 1972;
Cumberlidge and Uglow, 1977).
Furthermore, it was demonstrated that this coordinated response is the result
of a command system of interneurons, located in the circumesophageal
connectives innervating both the heart and gill bailers, whose activity can be
altered by sensory inputs with parallel changes in HR and ventilation rate
(Wilkens et al., 1974;
Field and Larimer, 1975a;
Field and Larimer, 1975b;
Taylor, 1982;
Miyazaki et al., 1985).
Interestingly, the most common responses to the stimulation of the command
fibers in these connectives are inhibitory in nature inducing bradycardia,
arrhythmia or heart arrest. In addition, stimulation of this command system
also elicits leg movements (Wilkens et
al., 1974). This command system may be the primary neural pathway
that enables the central pattern generators for ventilation and circulation to
be overridden by sensory input.
The fact that cardiac and escape responses are not necessarily triggered
together suggests a more complex relationship between them. When both
responses were elicited on perceiving a threat, a tight correlation was found.
However, bradycardia and not tachycardia was observed in
Chasmagnathus. This may seem counterintuitive and maladaptive since
the animals might be accumulating an oxygen debt when escape is starting. It
is well accepted that animals increase their ventilation rate and cardiac
output after a sudden stimulus (Wingfield,
2003) in a `fight or flight' reaction, and although animals across
many taxonomic groups have an alternate response to sudden stimuli that
includes decreased ventilation rate and decreased cardiac output, these
autonomic responses are normally correlated with behavioral freezing
(King and Adamo, 2006). The
prevalence of this alternate reaction across vertebrate and invertebrate
groups invites hypotheses that assume it has a universally adaptive function
related to `death feigning behavior' (McMahon and Wilkens, 1974;
Horridge, 1965); adaptive
metabolic drops (Burnett and Bridges,
1981); blood redistribution in preparation for flight
(Laming and Savage, 1980;
Laming and Austin, 1981;
King and Adamo, 2006).
Chasmagnathus, on the contrary, upon the presentation of sudden
and threatening stimulus, exhibits an initial burst of activity or startle
response presumably in an attempt to escape, though somewhat restricted by the
actometer, together with a strong CIR. This short lived activity as well as
the accompanying bradycardia lasts no longer than 10 s. Tachycardia may be
developing later or in a more natural setting. Guirguis and Wilkens
(Guirguis and Wilkens, 1995)
have stated that crustacean heart rate response to exercise involves two
phases. Phase I is rapid onset tachycardia, which occurs within the first
2–3 min of exercise. Most probably this occurs in
Chasmagnathus, but we have not yet explored responses beyond 10 s
after stimulus presentation.
The results obtained with virtual looming stimuli suggest that they are as
effective as more natural stimuli in eliciting cardiac responses and
applicable in research on the processes underlying the perceptual physiology
of invertebrates. Although it is generally acknowledged that many natural or
artificial threatening stimuli do not only elicit immediate overt defensive or
avoidance behavior, but also generate autonomic changes including rapid
changes in heart rate and blood pressure, few studies have been conducted in
invertebrates. In this work we found a clear correlation between cardiac and
escape response in Chasmagnathus to computer-generated looming
stimuli. Previous work on this crab had shown that a robust and reliable
escape response could be elicited by computer-generated looming stimuli while
two subclasses of previously identified movement-detector neurons from the
lobula (third optic neuropil) exhibited robust and consistent responses to the
same looming stimuli that trigger the behavioral response
(Oliva et al., 2007). These
effects were also studied in pigeons, showing a tight correlation between the
activity of the rotundal looming-sensitive cells, the muscle activity and the
heart rate measurements (Wang and Frost,
1992; Wu et al.,
2005). These findings and ours strengthen the idea that in the
face of impending danger the crab triggers several integrated defensive
reactions.
Although no response threshold differences were induced by the restrained condition, restrained crabs are more likely to respond to sensory stimulation. Although animals in both conditions showed a significant decrease in R2 for all the stimuli examined, differences in the probability of cardiac response were found between them. These might be related to differential attention states, as well as stress or sensitization imposed by the restrained condition.
The responses of the cardiovascular and respiratory systems in crustacea to
environmental and socially imposed alerting stimuli are very similar to the
responses of vertebrates mediated by the autonomic nervous system (ANS)
(Astley et al., 1991;
Cuadras, 1979;
Cuadras, 1980;
McMahon, 1995;
McMahon and Wilkens, 1983;
Li et al., 2000;
Listerman et al., 2000;
Schapker et al., 2002;
Shuranova and Burmistrov,
2002; Shuranova et al.,
2006). It is probable that the selective pressures that promoted
the development and maintenance of autonomic responses in the invertebrates
are the same for vertebrates. Recently it has been argued that although there
is no structural counterpart to the ANS in the invertebrates, the basic
functional properties of the ANS may have been established very early in
metazoan evolution (McMahon,
1995; Miller,
1997; Shimizu and Okabe,
2007). How the body plan developed such a system may have been
different in different taxa, but one would expect some similarities since the
crustacean autonomic responses are also neurally driven and regulated. In
addition, blood-borne hormones or compounds are released that influence many
target tissues at once. The involvement of the cardiovascular and respiratory
systems in this function has been conserved in evolution.
LIST OF SYMBOLS AND ABBREVIATIONS
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Aagaard, A., Styrishave, B., Warman, C. G. and Depledge, M. H. (2000). The use of cardiac monitoring in the assessment of mercury toxicity in the subtropical pebble crab Gaetice depressus (Brachyura: Grapsidae: Varuninae.). Sci. Mar. 64,381 -386.
Airriess, C. N. and McMahon, B. R. (1994). Cardiovascular adaptations enhance tolerance of environmental hypoxia in the crab Cancer magister. J. Exp. Biol. 190, 23-41.[Abstract]
Arechiga, H., Barrera-Mera, B. and Fuentes-Pardo, B. (1975). Habituation of mechanoreceptive interneurons in the crayfish. J. Neurobio. 6, 131-144.[CrossRef][Medline]
Astley, C. A., Smith, O. A. and Ray, R. D. (1991). Integrating behavior and cardiovascular responses: the code. Am. J. Physiol. 261,R172 -R181.[Medline]
Bloxham, M. J., Worsfold, P. J. and Depledge, M. H. (1999). Integrated biological and chemical monitoring: In situ physiological responses of freshwater crayfish to fluctuations in environmental ammonia concentrations. Ecotoxicology 8, 225-237.[CrossRef]
Burnett, L. W. and Bridges, C. R. (1981). The physiological properties and functions of ventilatory pauses in the crab Cancer pagurus. J. Comp. Physiol. 145, 81-88.
Camacho, J., Quadri, S. A., Wang, H. and Worden, M. K. (2006). Temperature acclimation alters cardiac performance in the lobster Homarus americanus. J. Comp. Physiol. A 192,1327 -1334.[CrossRef][Medline]
Chiussi, R. and Diaz, H. (2002). Orientation of the fiddler crab, Uca cumulanta: Responses to chemical and visual cues. J. Chem. Ecol. 28,1787 -1796.[CrossRef][Medline]
Cuadras, J. (1979). Heart rate and agonistic behavior in unrestrained crabs. Mar. Behav. Physiol. 6, 189-196.[CrossRef]
Cuadras, J. (1980). Cardiac responses to visual detection of movement, mechanostimulation and cheliped imposed movement in hermit crabs. Comp. Biochem. Physiol. A 66,113 -117.
Cumberlidge, N. and Uglow, R. F. (1977). Heart and scaphognathite activity in the shore crab Carcinus maenas. J. Exp. Mar. Biol. Ecol. 28, 87-107.[CrossRef]
Davis, M. (1992). The role of the amygdala in conditioned fear. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. J. P. Appleton), pp.255 -305. New York: Wiley-Liss.
Derby, C. D. (1982). Structure and function of articular sensillia of the lobster Homarus americanus. J. Crust. Biol. 2,1 -21.[Medline]
Diaz, H., Forward, R. B., Jr, Orihuela, B. and Rittschof, D. (1994). Chemically stimulated visual orientation and shape discrimination by the hermit crab Clibanarius vittatus (Bosc). J. Crust. Biol. 14,20 -26.[CrossRef]
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