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First published online August 8, 2008
Journal of Experimental Biology 211, 2600-2608 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016667
Spiny lobsters detect conspecific blood-borne alarm cues exclusively through olfactory sensilla
Department of Biology, Brains & Behavior Program and Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30303, USA
* Author for correspondence (e-mail: bioshs{at}langate.gsu.edu)
Accepted 27 May 2008
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Summary |
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Key words: chemoreception, Crustacea, olfaction
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INTRODUCTION |
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). Chemicals that
are actively released and signal alarm specifically among conspecifics are
known as alarm pheromones (Blum,
1985; Wyatt,
2003). For example, some social insects when attacked by intruders
use specialized glands to actively release alarm pheromones that signal to
conspecifics to defend their colonies
(Blum, 1985). These insect
colonies consist of genetically related individuals, and consequently these
alarm pheromones benefit signalers and receivers. In contrast, some animals
when injured by predators passively leak fluids that induce alarm behavior in
neighboring conspecifics, including social groups with little genetic
relatedness (Smith, 1992).
These chemicals, which benefit receivers but may not directly benefit the
sender, are called chemical alarm cues
(Seeley, 1995;
Viney and Franks, 2004).
Alarm pheromones are widespread across phyla but best studied in
arthropods; in particular, insects (Blum,
1985). Social insects release alarm pheromones when the colony is
threatened, inducing fighting or fleeing behavior from conspecifics
(Wyatt, 2003). Honeybees, for
example, release alarm pheromones from their specialized stinging apparatus to
recruit conspecifics to fight intruders
(Hunt et al., 2003;
Breed et al., 2004). This
stinging apparatus is autotomized onto the intruder, releasing alarm
pheromones that serve as a target for other attacking honeybees. Other insects
also use specialized glands to release alarm pheromones that trigger fighting
or fleeing behavior by conspecifics (Blum,
1985). The alarm pheromones mediate these behavioral responses
primarily through the insect's olfactory pathway
(Galizia et al., 1999;
Yamagata et al., 2006;
Yamagata et al., 2007).
Chemical alarm cues are used extensively by aquatic animals. These cues are
especially important during periods of activity such as foraging, when the
animal faces the greatest risk of predation
(Lima and Dill, 1990).
Chemical alarm cues leaked from injured or freshly killed conspecifics
indirectly indicate risk from active predators. Vertebrates such as fish
release alarm cues passively from fresh wounds in the skin
(Pfeiffer, 1977;
Smith, 1992;
Chivers and Smith, 1998). These
alarm cues in fish, like those in insects, are detected by the olfactory
system. Some fish have several olfactory pathways, with the one detecting
alarm cues being anatomically and functionally separate from those detecting
sex pheromones and food odors (Hamdani and
Døving, 2007).
The passive release of alarm cues during predation events is also frequent
in aquatic invertebrates. For example, sea urchins, sea snails, sea anemones
and crustaceans respond with alarm to chemical cues leaked from injured
conspecifics. Sea urchins, Diadema antillarum, respond to alarm cues
by moving away (Snyder and Snyder,
1970). Sea snails similarly respond by crawling or burrowing
(Snyder, 1967;
Jacobsen and Stabell, 2004).
Sea anemones respond to anthopleurine, a chemical that leaks from damaged
tentacles, by quickly retracting their tentacles
(Howe and Sheik, 1975).
Decapod crustaceans also respond with alarm behavior to fluids leaked from
injured conspecifics (Zimmer-Faust et al.,
1985; Rittschof et al.,
1992; Hazlett,
1994; Fleming et al.,
2007). Caribbean spiny lobsters, Panulirus argus, have
been reported to avoid fluids of injured conspecifics
(Parsons and Eggleston, 2005;
Parsons and Eggleston, 2006;
Bouwma, 2006;
Briones-Fourzán et al.,
2006; Briones-Fourzán
and Lozano-Álvarez, 2008). However, the source of chemical
alarm cues from injured conspecifics and the immediate behavioral responses to
such cues are poorly characterized. Furthermore, in decapod crustaceans in
general and Caribbean spiny lobsters in particular, the sensory mechanisms for
detecting chemical alarm cues are unknown. These crustaceans have dual
chemosensory pathways in their antennules, a major chemosensory organ
(Fig. 1). One of these pathways
is analogous to the olfactory pathway; it is based on aesthetasc sensilla,
which have dendrites of chemoreceptor neurons that project to the olfactory
lobes (Grünert and Ache,
1988; Schmidt and Ache,
1996a; Schmidt and Ache,
1996b). The other is a non-olfactory chemo-mechanosensory pathway;
it is innervated by the nine types of `non-aesthetasc' sensilla, which contain
both chemo- and mechanoreceptor neurons that project to the lateral antennular
neuropils and median antennular neuropil
(Schmidt and Ache, 1996a;
Schmidt and Ache, 1996b). The
aesthetasc–olfactory lobe pathway may uniquely process detection of
pheromones and other conspecific odors, whereas the
non-aesthetasc–lateral antennular neuropil pathway and the aesthetasc
pathway both detect general odors including food chemicals
(Gleeson, 1980; Gleeson, 1992;
Steullet et al., 2002;
Schmidt and Derby, 2005;
Johnson and Atema, 2005;
Horner et al., 2008a;
Horner et al., 2008b).
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MATERIALS AND METHODS |
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Chemical stimuli
Hemolymph was collected from P. argus, California spiny lobsters
Panulirus interruptus (Randall) or blue crabs Callinectes
sapidus (Rathbun), using a 3 ml syringe and needle (IM 11/2:
Becton Dickinson, Franklin Lakes, NJ, USA) inserted at the base of the fourth
or fifth leg. We used fresh hemolymph diluted 100 times with sea water (SW)
for each experimental day for most behavioral tests. Hemolymph diluted 300
times was used only for the behavioral assay on stimulus specificity because
it was as potent as hemolymph at 100 times dilution. SW was used as a negative
control stimulus in all experiments. Shrimp odor was used as a feeding
stimulus. It was prepared by blending shrimp tissue in SW at a concentration
of 2mgml–1, then filtering.
Ablation of sensilla
To determine whether the aesthetasc pathway is necessary or sufficient to
mediate alarm behavior, we performed behavioral experiments before and after
ablation of aesthetasc or non-aesthetasc sensilla. To test for the necessity
of aesthetascs, we performed behavioral tests during February and March of
2005 on 20 lobsters, first on all animals before treatment (`intact') and then
after either ablation of the aesthetasc pathway (nine lobsters) or sham
treatment (11 lobsters). Ablation of the aesthetascs was accomplished by
shaving the aesthetascs while sparing the non-aesthetasc sensilla on the
lateral flagellum and elsewhere. To shave the aesthetasc sensilla, we
immobilized the lobster, placed it in a plastic container (15 quart Nalgene
sterilisation pan; Lima, OH, USA; 38 cmx47 cm) filled with SW
15–20 cm deep under a dissecting light microscope, and shaved off
aesthetasc sensilla using a miniature scalpel. Control lobsters underwent the
same treatment, except that sensilla were left intact (sham treatment). After
treatment, both ablated and non-ablated lobsters were allowed to acclimate in
their aquaria for 1week before we performed the same behavioral experiments as
before treatment.
To test for the sufficiency of aesthetascs to mediate alarm responses, we performed behavioral tests during February of 2007 on 20 lobsters, first on all animals before treatment and then after either ablating the non-aesthetasc sensilla (10 lobsters) or sham treatments (10 lobsters). To remove non-aesthetasc sensilla, we immobilized lobsters as for aesthetasc ablation and then removed non-aesthetasc sensilla in multiple steps. First, we shaved all visible non-aesthetasc sensilla on the medial flagella and covered the remaining non-aesthetasc sensilla on the medial flagella with Superglue (Pacer Technology; Rancho Cucamonga, CA, USA; Superglue gel). Next, we shaved all visible non-aesthetasc sensilla on the lateral flagella, except for those in the aesthetasc tuft region, and then covered those surfaces with Superglue. We then shaved the remaining non-aesthetasc sensilla in the aesthetasc tuft region. Sham-treated lobsters were similarly immobilized but were only glued on antennular basal segments. Both ablated and non-ablated lobsters were then acclimated in their aquaria for 1 week before we resumed behavioral testing. In these experiments, concrete rectangular blocks (23 cmx23 cm) were used as shelters.
To determine the effectiveness of our sensillar ablations, we collected the
lobsters' antennular flagella after completing the behavioral assays according
to Schmidt and Derby (Schmidt and Derby,
2005). Flagella were removed and then fixed in 4% paraformaldehyde
(in 0.1 moll–1 Sorensen phosphate buffer + 15% sucrose, or
SPB) for 24 h. Flagella were then rinsed with SPB and stored in SPB with 0.02%
sodium azide until analyzed. To make 0.1 moll–1 SPB, we
dissolved 6.8 g KH2PO4 and 21.3 g
Na2HPO4 in 1l deionized H2O, adjusted the pH
to 7.4, and filtered the solution. For aesthetasc-ablated lobsters, we counted
the number of intact aesthetasc and asymmetric sensilla and damaged guard
sensilla. (Asymmetric and guard sensilla are in close proximity to the
aesthetasc sensilla and are thus sometimes damaged when shaving aesthetascs.)
For non-aesthetasc-ablated lobsters, we counted the number of intact
aesthetasc and non-aesthetasc sensilla on the lateral and medial flagella. For
both treatments, we calculated the percentage of intact and damaged sensilla
of the relevant types. Our analysis demonstrated the efficacy of the sensillar
ablations. In the aesthetasc-targeted group, 99.7±0.1% (mean ±
s.e.m.) of aesthetasc sensilla were ablated. In the process of ablating
aesthetascs, 52.1±3.4% (mean ± s.e.m.) of the asymmetric
sensilla and 3.2±0.6% (mean ± s.e.m.) of the guard sensilla were
damaged. In the non-aesthetasc-targeted group, we ablated 99.7±0.1%
(mean ± s.e.m.) of the non-aesthetasc sensilla, and 97.7±0.7%
(mean ± s.e.m.) of the asymmetric sensilla. In the process of ablating
the non-aesthetasc sensilla, 49.8±6.6% (mean ± s.e.m.) of the
aesthetasc sensilla were damaged.
Behavioral tests
The behavioral assay consisted of two phases: acclimation and test. The
acclimation phase consisted of giving lobsters at least 3–5 days to
become accustomed to the aquarium and behavioral testing protocol. This
included feeding lobsters a piece of shrimp using tongs and delivering SW or
diluted appetitive stimuli with glass pipettes. Lobsters learned to move
forward to appetitive stimuli (a small piece of shrimp or 1 ml of 2 or 200 mg
ml–1 shrimp odor) but not to negative controls (tongs without
shrimp or pipettes releasing 10 ml SW).
Following this acclimation phase, the test phase began, in which we measured appetitive and alarm behavioral responses to chemical stimuli, as defined below. In the test phase, we delivered 1–10 ml of 2mgml–1 shrimp odor, observed for 45 s, delivered 10 ml of an experimental stimulus (hemolymph) or control stimulus (SW), observed for 120 s, and then again delivered 1–10 ml of shrimp odor and observed for 30 s. All experimental events were video recorded (Sony DCR PC110) under low-intensity red light during the dark phase, and analyzed later.
We used three dependent measurements to assess the alarm response to hemolymph. The first measurement was a quantification of the occurrence and intensity of the alarm response of each animal during the 120s period following delivery of a chemical stimulus. Alarm responses include retreat, antennae whipping, high frequency shaking, leg shuffling and tail flipping (supplementary material Movies 1 and 2). The typical alarm response to physical threat or to alarm chemicals in our assay was retreat, in which a lobster curled its tail and walked backwards and away from the stimulus to a corner of the aquarium or inside the shelter. When backing into a corner, a lobster often raised its tail up against the aquarium wall while standing high on its front legs or firmly tucked its tail against the substrate while shuffling its front legs. Since retreat behavior was the most stereotypical and consistent alarm behavior, we used it as one dependent measurement of alarm response. The intensity of the alarm response according to our first dependent measurement was assessed using an ordinal scale, from –3 (most alarming) to 0 (no alarm; Table 1). Differences in intensity of the alarm responses toward control and experimental stimuli were tested for significance using non-parametric Wilcoxon matched-pairs tests. We also evaluated the data on a nominal scale, only evaluating whether or not an alarm response occurred. This allowed a simpler presentation of the data, and it is warranted because the conclusions based on analyses using ordinal and nominal measurements were very similar. According to the nominal scale, a response intensity of –1 or lower (Table 1) was rated as a `yes' for alarm response. Differences between nominal measurements were tested for significance using McNemar tests.
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The second dependent measurement of alarm was time spent in the shelter, expressed as a percentage of the 150 s time period after delivery of a stimulus. Statistical evaluation of differences in such ordinal data was achieved using Wilcoxon matched-pairs tests. A significantly greater percentage time in the shelter indicated that lobsters were alarmed by the stimulus.
The third dependent measurement was the suppression of the appetitive response to a food odor by hemolymph. An appetitive response is defined as the animal moving forward towards the source of the chemical. The intensity of the appetitive response to shrimp odor was measured on an ordinal scale from +3 (most attractive) to 0 (not attractive; Table 1). The intensity of the suppression of the appetitive response due to presentation of hemolymph was determined by comparing the intensity of the appetitive response before and after delivery of hemolymph. If the response to the first presentation of shrimp odor was significantly greater than the response to the second presentation of shrimp odor (which came after the presentation of hemolymph), then this was considered a suppression of the appetitive response. This statistical evaluation was made using Wilcoxon matched-pairs tests. We also used a nominal measurement of suppression of foraging by hemolymph, again because the conclusions using this simpler measurement were highly similar to those using nominal measurements. A response of 0 or lower to the second presentation of shrimp odor, after a response of +1 or greater to the first presentation of shrimp odor, was rated as suppression of the appetitive response by hemolymph. Differences between nominal measurements were tested for significance using McNemar tests.
Our data were collected in the course of three experiments. Our first experiment tested whether Caribbean spiny lobsters respond with alarm behavior when exposed to conspecific hemolymph before and after ablation of the aesthetasc sensilla. The control stimulus was SW. These two stimuli were delivered `blindfold' randomly over 2 days, with a maximum of two stimulus presentations per day per lobster. All three dependent measurements were used in this analysis.
Our second experiment tested whether spiny lobsters respond with alarm behavior when exposed to hemolymph before and after ablations of the non-aesthetasc sensilla. This was performed and evaluated in the same way as for the first experiment, except for the nature of the ablation.
Our third experiment tested the stimulus specificity of hemolymph in inducing either alarm or appetitive responses in P. argus. We examined behavioral responses to hemolymph from P. argus, P. interruptus and C. sapidus as experimental stimuli and SW as a control stimulus. We performed this experiment using two groups of lobsters, with three stimuli for each group. One group of lobsters was tested with P. argus hemolymph (positive control), SW (negative control) and P. interruptus hemolymph. A second group was tested with P. argus hemolymph, SW and C. sapidus hemolymph. This experiment was similar to the first two except that we did not present the second shrimp odor. Thus, in this experiment, we only used the first dependent measurement of alarm response to hemolymph, and did not use suppression of the appetitive response by hemolymph. Statistical significance was investigated using Cochran's Q test followed by McNemar tests for the related samples. To test for a significant difference between the alarm responses to hemolymph of C. sapidus and P. interruptus, we performed a Chi-squared test for independent measurements.
Field experiments
A field study was performed to determine whether wild Caribbean spiny
lobsters show the same alarm responses to hemolymph of conspecifics as animals
in the laboratory. The field study was performed in May–August of 2006
in the waters near the Florida Wildlife Commission facility in Marathon,
Florida. Lobsters were video recorded using an underwater microvideocamera
(Micro VideoTM Bobcaygeon, ON, Canada) mounted in a PVC pipe and
positioned approximately 1 m from the lobster. Recordings started at dusk,
around 19:30 h, and usually ended before 21:30 h. During this time, light
levels dropped sufficiently so that most lobsters left their dens and foraged
(Herrnkind et al., 1975). Some
of the recordings around 21:00 h required artificial illumination through two
IR illuminators (IR-200 ProVideo;
http://www.surveillance-video.com).
The IR illuminators were positioned directly above the surface of the water
and crevice site. We recorded from 18 sites, consisting of crevices of various
shapes and lobsters of varying numbers, all at approximately 1–3 m water
depth. Small crevices contained on average 3.3 lobsters. Stimuli were
delivered to lobsters through plastic tubes placed at each crevice site prior
to the behavioral experiments. We positioned the delivery end of the two
plastic tubes (0.4 mm i.d., 0.5 mm o.d.) approximately 0.3 m away from the
opening of each crevice site. The stimulus-loading end of the plastic tubes
was outside the water. One of these plastic tubes delivered the experimental
stimulus (hemolymph, diluted 100 times with filtered SW) and the other
delivered the control stimulus (filtered SW). Hemolymph was collected from
healthy lobsters by withdrawing it from the base of the fourth or fifth legs
using a syringe.
Our experiments had a paired design, with each lobster presented with two stimuli. SW, a negative control stimulus, was presented first, followed by a 3–4 min observation period. Then hemolymph was delivered, followed by another 3–4 min observation period. For each test, 60 ml of stimulus was delivered over 60–90 s. We chose to use this protocol rather than a randomized design because preliminary tests showed that animals first exposed to hemolymph often moved far enough away from the site of stimulus release that we were unable to present them with a second stimulus, whereas presentation of SW almost never produced this response. Thus, given our aim of using the power of a paired design, we always presented the SW negative control first.
All behavioral responses were recorded, with an emphasis on alarm responses observed in the laboratory experiments. These included moving away from the stimulus or moving into a shelter. Alarm responses were quantified as occurring or not (yes/no), as for laboratory experiments, by an evaluator blind to the nature of the stimulus delivered. Statistical differences between control and experimental stimuli were determined through paired McNemar tests.
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RESULTS |
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Lobsters with ablated aesthetascs reversed their behavior in response to hemolymph: instead of showing alarm responses, they showed appetitive feeding responses to hemolymph (Fig. 3A; supplementary material Movie 1). Before aesthetasc ablation, the percentage of lobsters showing appetitive responses to hemolymph was as low as to control stimuli. However, after ablation, this percentage increased significantly, to 100%. For sham-treated lobsters, the low percentage of animals that showed appetitive responses to hemolymph before treatment remained low after sham treatment.
Because aesthetasc-ablated lobsters engaged in appetitive responses instead of alarm responses when exposed to hemolymph, they spent significantly less time inside shelters than they did before ablation (Fig. 3B). After ablation, lobsters spent roughly equal time inside the shelter when exposed to either hemolymph or control stimuli (Fig. 3B). On the other hand, lobsters with sham treatment spent more time inside shelters in response to hemolymph than to control stimuli (Wilcoxon matched-pairs test, P>0.05; Fig. 3B).
Aesthetasc ablation strongly affected the ability of hemolymph to suppress appetitive responses to food chemicals (Fig. 3C). Before ablation, the percentage of lobsters that showed appetitive responses to shrimp odor was significantly higher when shrimp odor was presented after exposure to SW than after exposure to hemolymph. However, this suppression of the response to shrimp odor by hemolymph was eliminated following aesthetasc ablation. In contrast to ablated lobsters, sham-treated lobsters showed suppression by hemolymph. However, this suppression was not significantly different from suppression by SW (McNemar tests, P>0.05).
Non-aesthetasc ablation does not affect the alarm response
None of the four measurements of alarm responses to sources of alarm
chemicals changed after ablating non-aesthetasc sensilla
(Fig. 4). First, alarm
responses to hemolymph were not eliminated after non-aesthetasc ablation.
Following either experimental or sham ablation, responses to these stimuli
remained the same (Fig.
4A).
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Third, the amount of time that lobsters spent inside the shelter in response to hemolymph did not change after ablation of non-aesthetasc sensilla. Neither ablation nor sham treatment significantly changed the percentage of time spent inside the shelter following presentation of hemolymph (Fig. 4B).
Fourth, suppression of appetitive responses to shrimp odor by hemolymph did not change after ablation of non-aesthetasc sensilla. Neither ablation nor sham treatment changed the percentage of lobsters that were attracted to shrimp odor (Fig. 4C).
Stimulus specificity in the alarm response to hemolymph
The alarm response of Caribbean spiny lobsters, P. argus, was
greatest to hemolymph from conspecifics. The percentage of lobsters that
showed alarm responses was significantly higher with hemolymph from
conspecifics than with hemolymph from either California spiny lobsters, P.
interruptus, or blue crabs, C. sapidus
(Fig. 5). Interestingly,
hemolymph from P. interruptus evoked alarm responses in a
significantly greater percentage of lobsters than SW, whereas hemolymph from
C. sapidus did not (Fig.
5). Furthermore, appetitive responses of lobsters were
significantly lower to hemolymph from conspecifics compared with hemolymph
from either P. interruptus or C. sapidus (McNemar test,
P<0.05; N=20 and N=19, respectively;
Fig. 5), and C.
sapidus hemolymph induced appetitive responses in a significantly higher
percentage of lobsters than P. interruptus hemolymph (Fisher exact
test, P<0.05, N=19) or P. argus hemolymph.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)].
Our study complements previous studies by showing that spiny lobsters use
chemical alarm cues in both field and laboratory conditions. For example,
Caribbean spiny lobsters avoid shelters containing damaged conspecifics, both
in the laboratory and in the field
(Parsons and Eggleston, 2005;
Parsons and Eggleston, 2006;
Bouwma, 2006;
Briones-Fourzán et al.,
2006; Briones-Fourzán
and Lozano-Álvarez, 2008). Fishermen in Mexico avoid
throwing spiny lobster bodies back in the water after removing their tails
because this practice leads to a poor catch
(Briones-Fourzán et al.,
2006). California spiny lobsters avoid dens that contain leaked
fluids of fresh conspecific carcasses
(Zimmer-Faust et al., 1985).
Other crustacean species such as crayfish, hermit crabs and blue crabs also
avoid damaged conspecifics (Rittschof et
al., 1992; Hazlett,
1994; Acquistapace et al.,
2005; Ferner et al.,
2005).
Sensory pathways mediating alarm responses of spiny lobsters
This chemically induced alarm response is mediated by the olfactory
pathway. In spiny lobsters and other decapod crustaceans, the olfactory
pathway is represented by aesthetasc sensilla on the antennules, which contain
olfactory receptor neurons whose axons project to the olfactory lobes of the
brain (Fig. 1)
(Schmidt and Ache, 1996a;
Schmidt and Ache, 1996b). In
our study, the behavioral responses to hemolymph changed dramatically after
ablation of only the aesthetascs but not after ablation of all other
antennular sensilla (Figs3 and
4; supplementary material Movie
1). In fact, aesthetasc-ablated lobsters responded to hemolymph with very
different behavior from that of control lobsters: instead of retreating, they
walked forward and performed appetitive behaviors. A likely cause of this
response is that lobsters without aesthetasc sensilla detect food chemicals
but not alarm cues, both of which are present in the hemolymph, through the
non-aesthetasc sensilla. Indeed, it has previously been shown that either the
aesthetasc or non-aesthetasc pathway can mediate detection, discrimination and
orientation toward food odors (Steullet et
al., 2001; Steullet et al.,
2002). An alternate hypothesis is that aesthetasc-ablated lobsters
detect alarm chemicals but the pathways detecting them do not mediate alarm
responses.
Our finding that the aesthetasc pathway is necessary to mediate responses
to these intraspecific alarm cues is consistent with previous studies on
crustaceans showing that aesthetascs exclusively mediate behavioral responses
to conspecific odors. Male blue crabs with ablated aesthetascs show
significantly less courtship behavior in response to female urine-borne sex
pheromones than males with aesthetascs
(Gleeson, 1980;
Gleeson, 1982). American
lobsters and crayfish with ablated aesthetascs engage more frequently in
fights with dominant opponents, which use urine as an indicator of status,
than do those with aesthetascs (Johnson
and Atema, 2005; Horner et
al., 2008a). Caribbean spiny lobsters with ablated aesthetascs
show diminished preference to conspecific shelters containing urine-based
aggregation cues (Horner et al.,
2008b). Our study supports the view that spiny lobsters and other
decapod crustaceans have two functionally distinct antennular chemosensory
pathways: the aesthetasc pathway, uniquely for conspecific odors; and the
non-aesthetasc pathway, which together with the aesthetasc pathway mediates
responses to food and other general odors. Our study lays the foundation for
future studies of neural processing of alarm cues by the olfactory pathway of
spiny lobsters.
Species selectivity of alarm cues
The stereotypical alarm responses of Caribbean spiny lobsters were not
entirely specific to hemolymph of conspecifics. While hemolymph of
conspecifics induced almost exclusively alarm responses, hemolymph of
heterospecifics induced either similar alarm responses, though less frequent
or intense, or appetitive feeding responses
(Fig. 5). Hemolymph from the
more closely related Panulirus interruptus was more likely to produce
alarm responses from P. argus than was hemolymph from Callinectes
sapidus, which was more likely to evoke appetitive feeding responses.
Thus, our results suggest that hemolymph of P. argus has a
composition of chemicals that can alarm its conspecifics, and the ability of
heterospecific hemolymph to induce alarm responses in P. argus
depends on species relatedness. This idea is supported by recent results
(Briones-Fourzán and
Lozano-Álvarez, 2008) indicating that fluids of damaged
Panulirus guttatus, a close relative and sympatric to P.
argus (Ptacek et al.,
2001), induces similar avoidance responses in P. argus to
those induced by fluids of damaged P. argus. Differences in
effectiveness of the hemolymph from crustacean species might be due to either
the type or concentration of components in the hemolymph. Resolution of this
issue must await molecular identification of the alarm cues.
Predation risk assessment in decapod crustaceans
Spiny lobsters, like other aquatic animals, assess risk of predation and
use that information in determining their activity. During foraging, animals
face the highest risk of attack by predators
(Lima and Dill, 1990). Thus,
any assessment indicating the presence of active predators can dramatically
change an animal's foraging activity
(Wisenden, 2000). Spiny
lobsters forage predominantly at night under low light conditions, at which
time they rely heavily on their chemical senses for assessing risk while
trying to locate food, shelter or mates
(Herrnkind et al., 1975;
Kanciruk, 1980). If spiny
lobsters detect these cues when foraging, they are likely to move away from
that area and seek shelter. If they detect these cues when they are already in
shelters, they might move deeper into those shelters away from the source of
the alarm cues, or they might move to a nearby shelter away from the alarm
cues. Thus spiny lobsters tightly regulate foraging and any other activities
via the risk-assessment pathway – the olfactory pathway that
detects the chemical alarm cues.
This risk-assessment system coupled with an escape tactic represents an
effective evolutionary mechanism for reducing the risk of predation. Spiny
lobsters, like other crustaceans, autotomize their limbs to escape imminent
death from predators. Limb autotomy enhances escape and limits fluid loss from
wounds (Juanes and Smith,
1995; Fleming et al.,
2007), thus benefiting the individual performing it. In addition,
limb autotomy might benefit nearby conspecifics, if they can detect blood from
the autotomized limb and respond to its alarm cues by pre-emptively defending
themselves and avoiding areas containing active predators. This might be
considered as a form of predator tagging. We suggest that this might be a
mechanism by which this predator risk-assessment system has evolved.
Chemical alarm cues released from injured conspecifics might be transient,
as in the case of autotomy, or lingering. For example, some large predators
might consume a spiny lobster quickly and without much release of hemolymph,
in which case the alarm cue might be short lived. In other circumstances, such
as when a spiny lobster is damaged and leaking hemolymph or where a carcass is
slowly consumed by a predator, the alarm cue might be present in an area for a
longer time (Weiss et al.,
2008). In some species, chemical alarm cues can also end up
unaltered in predators' bodily excreta, such that conspecifics can detect
alarm cues released by the predator
(Chivers and Smith, 1998),
although such a means of tagging predators has not been demonstrated for spiny
lobsters or any other decapod crustacean.
Alarm pheromones or cues are almost exclusively used by animals that live
in groups, and since the organization of groups shows interspecific variation,
so do their responses to alarm pheromones
(Blum, 1985). In response to
alarm pheromones, some eusocial insects that form highly organized groups
fight aggressively with their chemical weaponry against predators
(Blum, 1985). Spiny lobsters
live in groups (Herrnkind et al.,
1975), but they lack the highly organized social colonies, close
genetic relatedness and chemical weaponry that social insects often have.
Accordingly, fleeing from blood-borne alarm cues, either into a solitary
shelter or towards other intact lobsters to form a group, is a highly adaptive
response for spiny lobsters because it reduces their risk of encountering
active predators. We suggest that this type of predation risk-assessment
system may be much more common and perhaps more complex than previously
thought in crustaceans and other arthropods.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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