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First published online November 19, 2007
Journal of Experimental Biology 210, 4150-4158 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.010173
Predator detection in Lymnaea stagnalis
Hotchkiss Brain Institute, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada, T2N 4N1
* Author for correspondence (e-mail: lukowiak{at}ucalgary.ca)
Accepted 18 September 2007
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Summary |
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Key words: Lymnaea, crayfish, sympatric predator, defensive behaviours, predator–prey interactions
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Introduction |
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). In
aquatic environments, chemical cues are important signals between and among
species (Alexander and Covich,
1991; Burks and Lodge,
2002; Chivers and Smith,
1998; Dodson,
1988) and provide a means by which organisms can gather
information about their spatio-temporal environment. Prey species utilize
olfactory detection of chemical cues to assess the risk of predation and thus
adjust their phenotype appropriately
(Hoverman and Relyea, 2007;
Kats and Dill, 1998;
Turner et al., 2000).
Many organisms, including gastropods, have been shown to use kairomones
[predator-derived chemical cues (Covich et
al., 1994; Jacobsen and
Stabell, 2004; Turner et al.,
2000)] for risk assessment, and as a consequence of this detection
increase the use of spatial or temporal refugia when predators are recognized
(Rigby and Jokela, 2000;
Vermeij and Covich, 1978).
Lymnaea stagnalis responds to both fish and crayfish
predator-released kairomones and, depending on the specific predator detected,
utilizes a functionally appropriate response by either sheltering under
crevices or crawling above the waterline
(Dalesman et al., 2006;
Rundle and Bronmark,
2001).
Learning about predators through pairing predation directly with the
predator or via damaged conspecific alarm cues or both has been noted in
several invertebrates including gastropods
(Chivers et al., 1996;
Hazlett et al., 2002;
Langerhans and Dewitt, 2002;
Rochette et al., 1998).
However, the majority of these studies utilized wild-caught animals, which
makes it impossible to determine whether predator-induced defence responses
were innate or the result of prior experience
(Dalesman et al., 2006). To
surmount this predicament, we set up an experimental protocol where only
snails from a population that has been maintained in the laboratory since the
early 1950s (i.e. over 250 generations) would be used. These snails would
therefore have never experienced a natural predator such as crayfish.
We have extensively utilized the Lymnaea model system to elucidate
the underlying neuronal mechanisms of: (1) the central pattern generator (CPG)
underlying aerial respiration; (2) how activation of the whole-body withdrawal
behaviour inhibits respiratory behaviour; (3) how learning and memory are
encoded within the nervous system; (4) how juvenile behaviours differ from
adult behaviour; and (5) how an environmentally relevant toxin
(H2S) alters adaptive behaviours
(Lukowiak et al., 1996;
McComb et al., 2002;
Parvez et al., 2006;
Rosenegger et al., 2004;
Syed et al., 1992b;
Syed and Winlow, 1991). We now
set out to determine, using this model system, how the detection of a predator
alters behaviour and the activity of neurons that control different aspects of
the behaviours.
Despite much investigation into predator–prey interactions in gastropods and specifically predator detection in Lymnaea stagnalis, few studies have examined empirically the behavioural and physiological manifestations of predator detection in this model organism. Our present study addressed the following questions. (1) Do laboratory-reared Lymnaea respond with predictable behavioural changes when exposed to predator effluent? (2) Does exposure to predator effluent induce metabolic changes in Lymnaea? (3) Does predator detection alter neuronal activity in key neurons involved in predator-induced defensive behaviours? Here our data unequivocally demonstrate that lab-bred Lymnaea are capable of detecting and responding in a functionally appropriate manner to the scent of a natural predator, the crayfish.
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Materials and methods |
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Righting response, exploratory behaviour and shadow withdrawal
We first sought to determine whether exposure to crayfish effluent (CE)
affected non-withdrawal defensive responses; therefore, we investigated two
measures of prey vigilance. When dislodged from the substrate and inverted
onto the dorsal surface of the shell, snails perform a righting behaviour to
regain contact with the substrate. We measured the time to right of individual
snails, first in pond water (PW) then, after 24 h, in CE water and boiled CE
(BC) following another 24 h rest interval. Individual snails were placed in a
9 cm Petri dish filled with 1 cm of PW, CE or BC water for a 10 min
acclimation period. A wooden stick was used to dislodge each snail and
manoeuvre it onto its dorsal surface. Each snail was dislodged 5 times and the
average righting time was taken in each treatment. To ensure that direction of
treatment was not a factor, treatments were run both in the order outlined and
in reverse.
As another measure of vigilance to predator presence, we determined the time to explore after full-body withdrawal in each treatment. When disturbed, snails withdraw into their shell and will re-emerge after a period and begin to explore when placed in PW. Snails were placed in a 1 l beaker filled with 500 ml of PW, CE or BC for 2 h, then withdrawn from the water and immediately placed into a 9 cm Petri dish filled with PW. The time to explore, as determined when the snail's tentacles and head were extended and the snail began to actively crawl along the substrate, was measured.
A third measure of predator detection that we analysed was to measure the
shadow-induced withdrawal response in Lymnaea. When performing aerial
respiration at the air–water interface, Lymnaea will close
their pneumostome (the respiratory orifice) and partially withdraw into their
shell, and thus inhibit aerial respiration, when a shadow passes over the
pneumostome opening (Stoll,
1973). We measured the shadow response of snails in PW, CE and BC
by passing a shadow over each snail during a bout of aerial respiration. A 35
W halogen light was placed 50 cm above 500 ml of PW, CE or BC in a 1 l beaker.
To increase the rate of aerial respiration, the water was made hypoxic by
bubbling N2 through it to displace the oxygen for 20 min prior to
placing the snails in the beaker. This is a standard procedure often utilized
during operant conditioning of the aerial respiratory behaviour (for details
see Lukowiak et al., 1996;
Lukowiak et al., 2003). Snails
were placed in the beaker and allowed to acclimate for 2 h. A 2 cm diameter
piece of cardboard was attached to the end of a stick and placed approximately
2–3 cm over an aerial respiring snail for 2–5 s. Withdrawal was
scored as successful if the snail completely closed the pneumostome under the
shadow within the 5 s interval. Each snail was tested 3 times and the mean
response was taken.
Brief description of aerial respiratory behaviour
Lymnaea are bimodal breathers obtaining oxygen either through
cutaneous respiration (i.e. directly through the skin) or through aerial
respiration via a rudimentary lung (i.e. gas exchange with the atmosphere). To
perform aerial respiration, the snail must surface and open its pneumostome
while contracting and relaxing the appropriate respiratory muscles. A more
detailed description has been given previously
(Lukowiak et al., 2003).
Breathing observations
To determine whether exposure to a crayfish predator affected the
respiratory behaviour, snails were first placed in 500 ml of room temperature
eumoxic pond water (PW) and then, after a 24 h rest interval, placed in 500 ml
of either CE or BC for 0.5 h. The time and duration of the pneumostome
openings were noted during each of the 0.5 h periods. From these measurements,
the number of openings, total breathing time and average breathing time were
calculated.
All experiments were done `blind' such that the examiner was unaware of the treatment being given.
Heart rate and O2 consumption
Heart rate was measured visually by observing the heart beating directly
through the shell. Snails were placed in a clear glass beaker containing 500
ml of PW or CE. The heartbeat was counted for 3x 1 min intervals and the
mean was taken. Two separate experimental procedures were utilized. (1) Snails
were allowed to acclimate in PW or CE for 10 min and then the heart rate was
counted. (2) Snails were placed in PW overnight and the heart rate was
measured in the morning, then the PW was siphoned out of the beaker and CE was
siphoned back in, such that the flow did not physically disturb the snails;
the heart rate was then measured in the same snails immediately after CE was
added. These two protocols were used to ensure that physically disturbing the
snails was not the cause of heart rate alterations and therefore were analysed
separately. Since the two protocols gave consistent results only data from the
latter are reported here.
Oxygen consumption was measured for snails in either PW or CE in a closed system. Individual snails were placed in a 50 ml Erlenmeyer flask filled with either PW or CE and all the air was flushed out when the rubber stopper was placed over the opening of the flask. An oxygen electrode was placed through the stopper and recordings were taken every 10 s for 20 min. Snails were rested for 24 h and then retested in the opposite treatment. Snails in both CE and PW were compared with `blank' controls where no snail was placed in the chamber, to account for electrode O2 consumption. Trials were stopped after 18–20 min to ensure that the level of oxygen in the chamber did not decrease beyond 90% saturation. O2 measurements were analysed using OxyView (PST3-V5.32 02/2004 by PreSens). Experiments were done at room temperature (22°C).
Semi-intact preparations
The preparations were dissected similar to methods previously described
(Inoue et al., 2001;
McComb et al., 2003;
Spencer et al., 1999) except
that only the penis was removed, the head/foot complex and buccal mass were
left fully intact. Preparations were pinned down in individual recording
dishes with their dorsal sides uppermost. The central ring ganglia (CNS) were
pinned to the dish directly through the foot musculature, dorsal-side up. The
outer sheath surrounding the CNS was removed using fine forceps. Standard
electrophysiological techniques were used as previously described in
Lymnaea semi-intact preparations. Intracellular recordings were
obtained using sharp glass microelectrodes filled with saturated
K2SO4 solution. Tip resistances of the microelectrodes
used for recordings ranged from 20 to 50 M
. Intracellular signals were
amplified via a NeuroData amplifier and displayed simultaneously on a
Macintosh PowerLab/4SP (ADInstruments) and a Hitachi oscilloscope. Recordings
were analysed and stored using the PowerLab software. See McComb et al.
(McComb et al., 2003;
McComb et al., 2005) for
fuller details.
Statistics
We analysed water treatment effects on snail behaviour data with repeated
measures analysis of variance. All repeated measures data were tested for
equal variance using Mauchly's test for sphericity. In cases where sphericity
could not be assumed, we used the conservative adjusted Greenhouse-Geisser
P values. For cases in which we identified a significant interaction
between the repeated factor and water treatment, we used repeated contrasts to
identify which water treatment pairs differed significantly. For oxygen
consumption experiments, we paired averaged time-matched O2
saturation values for each snail in both PW and CE treatments.
Electrophysiological data were analysed using ANOVA with Tukey's post
hoc test to detect cases in which we identified a significant
interaction. Non-homogenous data (number of spikes per 10 min interval) were
square-root transformed to homogenize data prior to ANOVA. All statistics were
performed on SPSS version 11.0.4 for Macintosh.
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Breathing observations
We next determined whether aerial respiratory behaviour was altered in
Lymnaea exposed to CE. Previous reports indicate that when pulmonate
snails are in the presence of a crayfish predator they tend to spend more time
near the surface of the water (Dalesman et
al., 2006; Turner et al.,
2000; Turner and Montgomery,
2003). We hypothesized that if our laboratory-reared
Lymnaea were capable of detecting crayfish kairomone, and as a
consequence spent more time at the air–water interface, they may show a
significant alteration in aerial respiratory behaviour. We therefore measured
the number of pneumostome openings and the total breathing time in PW, CE and
BC. These data are plotted in Fig.
4. As can be seen, the number of pneumostome openings
(Fig. 4A) and the total
breathing time (Fig. 4B) were
significantly increased in CE (P<0.01, N=65) compared
with controls. Interestingly, the mean breathing time for each pneumostome
opening was not significantly different as a result of CE exposure
(Fig. 4C, P=0.144,
N=65). We conclude that snails can detect the presence of a crayfish
predator and increase the number of times they open their pneumostome to
breathe, and thereby increase the total breathing time when exposed to CE.
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Non-aerial oxygen consumption (i.e. cutaneous respiration) was measured in
both PW and CE by analysing the rate of oxygen decrease over time in a closed
system (see Materials and methods). We found that the mean O2
consumption was not significantly different between the two treatments (i.e.
PW vs CE) over the course of the experiment. However, we found a
significant increase in O2 consumption in PW-treated snails between
2 and 8 min (Fig. 5A). It is of
note that between the 4 and 8 min time points the averaged data give the
appearance of a small increase in percentage saturation. However, in fact the
oxygen level in the chamber does not increase for any one animal and this
apparent increase in percentage saturation is explained by the noticeable
increase in variation of animal behaviour during this time period (see
Discussion). By taking the ratio of CE to PW O2 consumption for
each snail at each time interval, a striking 3-fold increase in O2
consumption in the PW-treated snails compared with CE-treated snails was
detected during this time interval (Fig.
5B). Therefore, we found that there was a time-dependent increase
in O2 consumption in PW that was not apparent in CE. That is,
snails in CE do not consume O2 as rapidly as snails in PW during
the initial stage of the experiment. This suggests to us that in
Lymnaea the so-called compensatory mechanisms described by Taylor et
al. (Taylor et al., 2003)
during exposure to a hypoxic challenge are suppressed by the detection of the
predator.
Electrophysiological activity of RPeD1
Finally, we examined the activity of RPeD1 in semi-intact preparations that
had previously been treated with PW, CE or BC. We chose RPeD1 because this is
the neuron that (1) initiates the rhythmic activity that drives aerial
respiratory behaviour and (2) is inhibited during the defensive full-body
withdrawal response. We found significant reductions in three measures of
activity in the CE-treated animals compared with either the PW- or BC-treated
snails (Fig. 6). The
spontaneous firing activity, bursting activity and number of spikes per burst
in CE-treated snails were significantly reduced compared with those in the PW-
and BC-treated snails. Representative samples of recordings taken from RPeD1
in PW, CE and BC are presented in Fig.
6A, whilst summary data are presented in
Fig. 6B,C. As is readily
apparent, exposure of the intact snail to CE for 2 h before dissection was
sufficient to significantly alter on-going electrical activity in RPeD1. We
found no significant differences in other electrophysiological parameters (see
Table 1) such as resting
membrane potential, action potential amplitude or after-hyperpolarization.
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;
Levri, 1998;
McCarthy and Fisher, 2000;
Turner, 1997). However, our
inability to detect changes in heart rate for snails in the presence of CE
suggests that the increase in aerial respiratory behaviour may simply be a
result of spending more time near the air–water interface and not due to
increased respiratory demand. In support of this suggestion are our data
showing that snails in PW initially consume more O2 via cutaneous
respiration than they do in CE (Fig.
5); although at the end of the experiment the two groups had
consumed the same amount of O2. Therefore, it appears that
detection of the predator alters the so-called `compensatory' response of an
organism to hypoxia. As has been pointed out in other publications
(Taylor et al., 2003;
Taylor et al., 2001),
organisms when sensing a decrease in PO2
initially increase behaviours (the `compensatory response') such as heart rate
and respiratory rate to counteract the fall in
PO2. Snails that sensed the predator did not do
this and therefore we expect that these adaptive responses may represent an
attempt to minimize O2 requirements, and thereby lessen or avoid
hypoxic impairment or damage (Hochachka et
al., 1996). How this suppression of the compensatory response is
mediated in the snail is not clear but will be the subject of further
investigation. The above results combined with our findings of significant
suppression of exploratory behaviour and a significant increase in the
righting response following CE exposure (Figs
1 and
2) suggests that snails
detecting the predator (i.e. increased risk assessment) alter their activities
in a manner consistent with behavioural decisions that would prove beneficial
to survivorship (i.e. `keeping a low profile' or getting out of harm's way
quicker). This is not surprising given that predator detection via kairomones
not only gives information regarding predator presence but also potentially
gives information regarding the proximity, physiological state and even diet
of potential predators (Dalesman et al.,
2006; Kats and Dill,
1998; Wisenden,
2000).
Exposure to predator odour from crayfish (i.e. CE) also caused a
significant increase in the shadow response compared with controls
(Fig. 3). Further, the righting
response time of snails exposed to CE was decreased compared with either pond
or boiled crayfish water (Fig.
1). Collectively these data sets indicate that snails actively
reduced the duration of vulnerability on perceiving the presence of a
predator. Increases in anti-predator responses such as vigilance during times
of predator presence have been demonstrated in many aquatic organisms in which
prey respond appropriately to factors such as predator density
(Wiackowski and Staronska,
1999), distance (Turner and
Montgomery, 2003), size of predator and prey vulnerability
(Alexander and Covich, 1991;
Cotton et al., 2004;
Dewitt et al., 1999). Multiple
prey traits allowing for functional responses to predator threat are not
uncommon in aquatic systems as multiple traits provide a battery of possible
defences against predation. Lymnaea and other pulmonates are capable
of altering their defensive responses appropriately according the perceived
predator threat. That is, depending on `who' the predator is (e.g. fish
vs crayfish), a different defensive strategy will be taken.
Differential habitat use under multiple predator systems demonstrates both
increased vigilance and the differentiation between predator threats, allowing
for functional tradeoffs in predator defence
(Dalesman et al., 2006;
Dewitt and Langerhans,
2003).
When naïve snails were exposed to CE, the spontaneous firing activity
and bursting activity of RPeD1 decreased in the semi-intact preparations
compared with control snails (Fig.
6). To our knowledge this investigation provides the first
evidence of neurobiological changes associated with predator detection in
pulmonates. RPeD1 has been shown to be both necessary and sufficient to drive
the aerial respiratory behaviour of Lymnaea
(Syed et al., 1992a;
Syed and Winlow, 1991) and is
subordinate to the defensive full-body withdrawal behaviour
(Inoue et al., 1996;
Syed and Winlow, 1991). It is
therefore not surprising that the activity pattern of this neuron is altered
in the manner described when the crayfish predator is detected.
Neurobiological investigation of the shadow response in Lymnaea has
demonstrated that this process is mediated by peripherally located dermal
photoreceptors and is susceptible to the habituation phenomenon
(Stoll, 1973). It is therefore
feasible that detection of a predator alters both central (RPeD1) and
peripherally located components of the aerial respiratory network. The
apparent conflict in our data showing an increase in respiratory behaviour and
a decrease in the activity of RPeD1 may be explained by an up-regulation in
the efficacy of peripheral inputs onto downstream components of the
respiratory network, which would therefore require less input from RPeD1 to
initiate the respiratory rhythm. Further investigation into both the location
and activity of these chemosensory receptors is ongoing in our laboratory.
Previously it has been demonstrated that there is an age-dependent change in
suppressive input from the pneumostome area to CNS neurons, such as RPeD1
(McComb et al., 2005). Thus,
we do not find it surprising that alterations in the peripheral nervous system
function as a result of predator detection, and may play an important role in
the mediation of aerial respiratory behaviours. The interaction between the
central and peripheral nervous systems of molluscs, especially as regards
mediation of adaptive behaviours, is complicated, interesting and
controversial (Lukowiak and Colebrook,
1988; Lukowiak and Jacklet,
1972).
Lymnaea stagnalis has been extensively investigated as a model
demonstrating the neuronal basis of cue-associated learning
(Benjamin et al., 2000;
Haney and Lukowiak, 2001;
Sugai et al., 2007;
Sugai et al., 2006); however,
ours is the first study to investigate how a naturally occurring and
ecologically relevant chemical cue alters neuronal function in
Lymnaea. Further, the neuronal and molecular changes associated with
operant conditioning of the respiratory behaviour in Lymnaea have
been demonstrated in RPeD1 and therefore make this neuron the prime candidate
for investigation of the neuronal mechanisms of `fear conditioning' in an
identified neuron.
Together, our data demonstrate numerous defensive behavioural and
physiological responses that Lymnaea utilize following detection of a
predator scent. The data also unequivocally show that this instinct has been
maintained in the lab-reared snails over many generations and may allow
investigations at the neuronal level into how such instinct is mediated. These
behaviours are robust and repeatable in the laboratory setting and support
both laboratory and field investigations demonstrating that Lymnaea
stagnalis not only detect predator kairomones but also respond in the
appropriate manner to decrease the probability of predation. The identity of
these kairomones has yet to be elucidated; however, chemical communication
within decopod crustaceans is well described
(Ameyawakumfi and Hazlett,
1975; Atema, 1986;
Blake and Hart, 1993), and a
metabolic component within the urine has been shown to play a role in
dominance hierarchies (Breithaupt and Eger,
2002; Schneider et al.,
1999). It is therefore likely that a component within the urine is
a candidate for the kairomone involved in these snail–crayfish
interactions.
The mechanisms of predator detection, which presumably are crucial to
survival, remain hard to elucidate because of the difficulty in demonstrating
causal links (Bolhuis and Macphail,
2001) between ecologically relevant behaviours
(Kavaliers and Choleris, 2001)
and neural substrates driving these behaviours. We have begun to form these
links by investigating ecologically relevant chemical cues and the associated
neuronal networks that are affected by predator detection. Since the molecular
events in a single neuron (RPeD1) in Lymnaea have been shown to be
necessary for long-tem memory formation, reconsolidation, extinction and
forgetting (for reviews, see Lattal et
al., 2006; Parvez et al.,
2006), it is now possible to directly investigate how an
ecologically relevant stress stimulus that has been maintained in
laboratory-rearing conditions affects learning and memory at the level of a
single neuron.
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