Download DIFFERENCES IN MEMORY CAPABILITIES IN INVASIVE AND

JOURNAL OF CRUSTACEAN BIOLOGY, 22(2): 439–448, 2002
DIFFERENCES IN MEMORY CAPABILITIES IN INVASIVE AND
NATIVE CRAYFISH
Brian A. Hazlett, Patrizia Acquistapace, and Francesca Gherardi
(BAH, correspondence) Department of Biology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
([email protected]); (PA, FG) Dipartimento di Biologia Animale e Genetica ‘Leo Pardi’,
Universitá di Firenze, Via Romana 17, 50125, Firenze, Italy
A B S T R A C T
The memory capabilities of individuals of four species of crayfish (two invasive species and two
native species) were tested in the laboratory. Individuals of the invasive Orconectes rusticus and
the native O. virilis were tested in Michigan, and the invasive Procambarus clarkii and the native
Austropatmobius pallipes were tested in Italy. Following pairing of conspecific alarm odour and a
novel odour (goldfish odour), individuals were tested one day, one week, and either three weeks
later (Italy) or two and four weeks later (Michigan) for inhibition of feeding responses by goldfish
odour. In all four species, exposure of animals for just two hours was sufficient to establish an association between the novel odour and elevated predation risk. In both species pairs, individuals of
the invasive species showed evidence of retention of the learned association longer than did individuals of the native species. The results are consistent with the general hypothesis that invasive
species have a greater capacity for behavioural plasticity.
Avoiding predation is of obvious importance for individuals of all species. While
some animals respond to cues associated with
elevated predation risk without past experience with those cues (conspecific alarm
odour, Hazlett and Schoolmaster, 1998), most
studies have indicated that learning is involved in the recognition of danger cues. Experience is necessary for recognition of
predator odour in the minnow Pimephales
promelas (see Mathias and Smith, 1993a) as
well as for other species of fish (Magurran,
1989; Chivers et al., 1995). Chivers et al.
(1996) demonstrated that a similar experiential requirement held for the damselfly, Enallagma species. Hazlett and Schoolmaster
(1998) showed that at least some species of
crayfish show predation avoidance responses
to the introduction of the odour of predators
only after such odours have been paired with
alarm odours. In some cases, naïve individuals can learn to respond to predator cues from
experienced individuals (Mathias et al., 1996).
Aggressiveness may be associated with invasive species (Capelli and Munjal, 1982;
Hill and Lodge, 1999); however, few studies
have directly compared other aspects of the
behaviour of invasive species and the native
species they have displaced. In the case of
species introduced to a new habitat, which is
likely to contain predators not encountered in
their former range, efficient learning about
cues associated with elevated predation risk
would seem to be especially critical. It is reasonable to suggest that successful invaders
will exhibit a higher degree of plasticity in a
number of behaviours (Hazlett, 2000a), including learning about predator cues and thus
reducing predation risk (Mathias and Smith,
1993b).
We tested these general predictions in two
pairs of crayfish: the invasive Orconectes rusticus (Girard, 1852), an Appalachian drainage
species, and the native species it has displaced
in many parts of the midwest U.S.A. and
Canada, Orconectes virilis (Hagen, 1870)
(Garvey et al., 1994; Hill and Lodge, 1999)
and the southern U.S.A. invasive Procambarus clarkii (Girard, 1852) and a native Italian species Austropotamobius pallipes
(Lerebboullet, 1858) which is threatened in
southern Europe by P. clarkii (Gherardi et al.,
1999). In particular, we tested the predictions
that species that are successful invaders
should learn associations faster and remember those learned associations longer than native species that are not known to be successful invaders.
MATERIALS AND METHODS
The Orconectes species were studied in the laboratory in Ann Arbor, Michican, U.S.A., in September and
439
440
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 2, 2002
October, 2000. The Procambarus clarkii and Austropotamobius pallipes were studied in the laboratory in
Florence, Italy, in June and July, 2000. The same methodology was used for both species pairs. Individuals of O.
rusticus were collected from Burt Lake, Michigan, while
the O. virilis were collected from the ponds at the DNR
Fisheries Station in Saline, Michigan. The P. clarkii were
collected from Padule di Fucecchio, a freshwater swamp
60 km from Florence, while the A. pallipes were collected
from Fosso di Farfereta, a third-order stream 40 km from
Florence. All individuals used were adults and approximately equal numbers of both sexes were used. All crayfish were fed pieces of freeze-thawed cod fish prior to the
initiation of training and testing.
Following the method of Chivers and Smith (1994),
the crayfish were trained with a novel odour, the odour
of the common goldfish, Carassius auratus. None of the
crayfish would have encountered this species in the field,
and because C. auratus is an herbivore it is not a potential predator. Control animals were tested with goldfish
odour (see below) without any prior exposure to that
odour. Test animals were trained with either a short experience or a long experience with a combination of conspecific alarm odour and goldfish odour. The short experience consisted of placing two medium-size (30-mm
standard length) goldfish in an opaque plastic container
that had many holes drilled in the side into a communal
aquarium containing the crayfish for two hours. At the beginning of the 2-h period, and after 1 h, conspecific alarm
odour was slowly poured into the water. Conspecific
alarm odour was prepared by crushing a medium-size
(20–25-mm cephalothorax length) conspecific individual
in 150 ml of water and filtering with coarse filter paper.
In the case of the long-experience test individuals, the
goldfish were left in the communal aquarium with the
crayfish for 24 h, and an additional application of alarm
odour was added 18 h after the first two applications.
Immediately after the training period, crayfish were
placed in individual containers. These containers were visually isolated from each other and contained 15 litres
of continually aerated well water and half of a clay pot
to serve as a shelter. Crayfish were tested after 24-h acclimation in the observation aquaria. Behaviours were observed and recorded on a personal computer with an event
program. As in Hazlett (1999), the parameters recorded
were: (a) time in shelter, (b) time spent in locomotion
by movement of the ambulatory legs, (c) time spent executing cleaning movements, (d) time spent executing
feeding movements of the chelipeds and chelate walking
legs, and (e) time in one of three postures: raised, intermediate, or lowered. These latter postures were characterised in the following ways: in the raised posture the
body was elevated off the substrate, the chelipeds were
held off the substrate parallel to the substrate or higher,
and the abdomen and telson were extended; in the intermediate posture, the body was held just off the substrate,
the tips of the chelipeds were lightly touching the substrate and the telson was perpendicular to the substrate;
in the lowered posture, the body was in contact with the
substrate, the chelipeds were drawn in towards the body,
and the telson curled under the abdomen. Individuals
could move both while in and out of the shelter; thus,
those categories of behaviour are independent measures.
Because an animal had to be in one of the three postures,
the times in those postures are not independent, and only
times spent in the raised and lowered postures were
analysed.
Each crayfish was observed during a two-minute control period following the introduction of 5 ml of well
water, then a 2-min period following the introduction of
5 ml of food odour, and immediately following that, a
2-min period following the introduction of 5 ml of goldfish odour. All solutions were introduced via a syringe.
Earlier studies (Hazlett, 1999; Bouwma and Hazlett,
2001) suggest that the use of two, potentially conflicting
stimuli yields more sensitive measures of changes in behaviour and reception of stimuli than presentation of a
single stimulus.
Food odour was generated by macerating 200 g of
freeze-thawed cod in 150 ml of well water. Goldfish odour
was generated by placing two medium-size goldfish in
two litres of well water for 24 h prior to use in testing.
After the initial testing, crayfish were returned to communal tanks and the individual observation tanks were
cleaned and refilled with well water. The Orconectes
species were tested again 1, 2, and 4 weeks after the initial tests, while P. clarkii and A. pallipes were tested again
1 and 3 weeks after initial testing. The scheduling of other
observations dictated the different patterns in Michigan
and Italy. Ten individuals of each species and experience
treatment (control, short experience, long experience)
were tested. Mortality resulted in a sample size of 8 or 9
in some of the later tests for several species × treatment
categories. Obviously the repeated testing of the same individuals with just goldfish odour will affect the rate of
memory decay (Dukas, 1998). However, all individuals of
all species were treated in the same way, and the comparisons of interest were between the species of crayfish.
For each crayfish, the number of seconds spent in the
various behaviours during the three test conditions (control, food odour, goldfish odour) on a given test day were
extracted from the event recorder files. An ANOVA was
used to test for a treatment effect on each behaviour, and
only for those behaviours with a significant treatment effect (P < 0.05) the Tukey test was used for pairwise comparisons of the three treatments. These analyses were conducted for each species, for both experience durations,
for each date. Where the number of seconds spent in behaviours was different for food-odour periods and goldfish-odour periods, this was taken as evidence of an effect of the goldfish odour on food-related responses. That
is, when the addition of goldfish odour significantly depressed the levels of food-related responses, we judged
that the crayfish had treated goldfish odour as a cue related to potential predation risk. Similar patterns of the
depression of feeding responses by detection of the odour
of real predators have been reported for other species of
crayfish (Blake and Hart, 1993; Hazlett and Schoolmaster, 1998; Hazlett, 1999; Bouwma and Hazlett, 2001).
RESULTS
In all species tested, the behaviours that
differed most consistently among control and
the two test periods (food alone, goldfish +
food odour) were feeding, locomotion, and
time in the raised posture. The other behaviours or categories (cleaning, time in shelter,
and time in the lowered posture) did not differ among odour treatments for the vast majority of cases and were judged not to be good
measures of the response to test stimuli. Thus,
HAZLETT ET AL.: MEMORY CAPABILITIES IN CRAYFISH
441
these behavioural measures were not used in
looking for an effect of goldfish odour.
Orconectes rusticus and Orconectes virilis
When food odour was introduced, the control animals in both species showed a significant increase in at least some of the behaviours related to feeding (feeding, locomotion,
and raised posture) compared to control periods. When goldfish odour was introduced
there was no change in behaviour and the animals continued to show feeding behaviours
at the same level as when food odour alone
was introduced (Fig. 1). Thus, animals that
had had no experience with goldfish odour
did not change their behaviour when that
odour was introduced.
Tests One Day After Training.—For both
species and both experience durations, when
tested one day after training, crayfish responded to the introduction of goldfish odour
by a significant reduction in the number of
seconds spent in at least some food-related
activities (Fig. 2; Tables 1, 2). In both species
and for both experience treatments, feeding
was reduced to control levels (Fig. 2). In the
case of O. rusticus with short experience, this
was true also for raised posture. For longexperience O. rusticus, three behaviours
(feeding, locomotion, and raised posture)
were significantly affected and the levels reduced to control-period durations (Table 1).
Short-experience O. virilis showed significant
reduction in feeding, locomotion, and raised
posture compared to food-alone treatments,
and there was no difference between goldfish odour added and control periods. Longexperience O. virilis showed a significant reduction only in feeding (Table 2).
Tests One Week After Training.—When tested
one week after training, both the shortexperience and long-experience individuals
of the invasive species, O. rusticus, showed
significant reductions in the time spent feeding (Fig. 2), locomoting, and in the raised
posture when goldfish odour was introduced
(Table 1). The short-experience individuals of
the native species, O. virilis, appeared to have
forgotten after one week as there were no significant reductions in any behaviours following introduction of goldfish odour (Table 2),
and these animals were not tested further. For
the long-experience O. virilis both feeding
Fig. 1. Number of seconds (mean + SE) spent by control animals of (A) Orconectes rusticus and (B) Orconectes virilis in three activities under different odour
treatment conditions. For each behaviour, different letters
indicate significant differences between odour treatments
by Tukey tests (P < 0.05).
(Fig. 2) and locomotion showed marginal differences between food odour alone and goldfish odour conditions, but there was clearly
no difference between goldfish odour and
control conditions.
Tests Two Weeks After Training.—For the
short-experience O. rusticus, there were significant reductions for feeding (Fig. 2) and
locomotion (Table 1), whereas for the longexperience O. rusticus the reductions following introduction of goldfish odour were
significant for feeding (Fig. 2), locomotion,
and raised posture (Table 1).
442
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 2, 2002
Fig. 2. Number of seconds (mean + SE) spent in feeding behaviours for (A) Orconectes rusticus, short experience,
(B) O. rusticus, long experience, (C) Orconectes virilis, short experience, and (D) O. virilis, long experience. Data
are presented for the three odour conditions at different times after experiencing the pairing of goldfish odour and
conspecific alarm odour for either two hours (short-experience animals) or 24 hours (long-experience animals). Different letters indicate significant differences between odour treatments during a given time since training (Tukey
tests, P < 0.05).
In the case of the long-experience O. virilis there were no changes in feeding-related
behaviours when goldfish odour was introduced (Table 2), and thus the association between alarm odour and goldfish odour was no
longer detectable. These crayfish were not
tested further.
in feeding activities (Fig. 2) or any other
behaviours following the introduction of
goldfish odour (Table 1). This pattern was observed also for the long-experience individuals of O. rusticus (Table 1). Thus, all of the
crayfish had apparently forgotten the learned
association by four weeks after training.
Tests Four Weeks After Training.—When
tested four weeks after the initial training, the
individuals of O. rusticus that had had the
short experience did not show any change
Procambarus clarkii and
Austropotamobius pallipes
For the control animals that had not had
prior exposure to goldfish odour, individuals
HAZLETT ET AL.: MEMORY CAPABILITIES IN CRAYFISH
443
Table 1. Results from Tukey tests (probability values) comparing the time spent in 3 behaviours (feeding, locomotion,
raised posture) in response to pairs of odour treatments (control vs. food odour, food odour vs. goldfish odour, and
control vs. goldfish odour) by individuals of Orconectes rusticus. Results are presented separately for animals with short
experience (2 h of pairing of goldfish odour and alarm odour) and long experience (24 h of pairing of goldfish odour and
alarm odour). Results from Tukey tests are reported only for behaviours in which the overall ANOVA showed a
significant difference (P < 0.05).
Short-experience O. rusticus
1 day after training
Feeding
Locomotion
Raised posture
1 week after training
Feeding
Locomotion
Raised posture
2 weeks after training
Feeding
Locomotion
Raised posture
4 weeks after training
Feeding
Locomotion
Raised posture
Long-experience O. rusticus
Control-Food
Food-Goldfish
Control-Goldfish
Control-Food
0.001
–
0.014
0.001
–
0.022
0.896
–
0.979
0.001
0.001
0.001
0.001
0.001
0.003
0.292
0.650
0.827
0.001
0.010
0.012
0.002
0.047
0.024
0.825
0.773
0.945
0.001
0.005
0.009
0.001
0.056
0.074
0.530
0.578
0.619
0.001
0.007
–
0.001
0.014
–
0.975
0.953
–
0.001
0.021
0.013
0.001
0.058
0.044
0.847
0.892
0.847
0.008
–
–
0.861
–
–
0.027
–
–
0.015
0.025
0.08
0.984
0.997
0.893
0.010
0.025
0.031
of both species showed strong increases in
feeding, locomotion, and time in the raised
posture when food odours were introduced,
and there were no changes in those behaviours when goldfish odour was introduced
(Fig. 3). The crayfish continued to show high
levels of feeding-related activities during the
period following goldfish-odour introduction,
indicating that naïve animals did not treat
goldfish odour as a cue related to possible
predation risk.
Food-Goldfish Control-Goldfish
Tests One Day After Training.—Individuals
of Procambarus clarkii showed significant
reductions of all three feeding-related behaviours when goldfish odour was introduced for
the long-experience animals (Fig. 4; Table 3).
For locomotion and raised posture the time
spent when goldfish odour was introduced
was significantly lower than when food
odours alone were present but also significantly higher than during control periods. For
the short-experience P. clarkii, the reductions
Table 2. Results from Tukey tests (probability values) comparing the time spent in 3 behaviours (feeding, locomotion,
raised posture) in response to pairs of odour treatments (control vs. food odour, food odour vs. goldfish odour, and
control vs. goldfish odour) by individuals of Orconectes virilis. Results are presented separately for animals with short
experience (2 h of pairing of goldfish odour and alarm odour) and long experience (24 h of pairing of goldfish odour and
alarm odour). Results from Tukey tests are reported only for behaviours in which the overall ANOVA showed a
significant difference (P < 0.05).
Short-experience O. virilis
1 day after training
Feeding
Locomotion
Raised posture
1 week after training
Feeding
Locomotion
Raised posture
2 weeks after training
Feeding
Locomotion
Raised posture
a
experiment not conducted
Long-experience O. virilis
Control-Food
Food-Goldfish
Control-Goldfish
Control-Food
Food-Goldfish Control-Goldfish
0.001
0.001
0.007
0.001
0.002
0.012
0.934
0.916
0.966
0.002
–
–
0.003
–
–
0.975
–
–
0.003
0.023
0.032
0.295
0.575
0.674
0.075
0.174
0.169
0.005
0.009
–
0.077
0.079
–
0.477
0.600
–
a
a
a
a
a
a
a
a
a
0.028
0.023
–
0.964
0.629
–
0.048
0.150
–
444
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 2, 2002
after the initial training, showed significant
reductions in feeding (Fig. 4) and time in
raised posture when goldfish odour was introduced (Table 3). For the long-experience
P. clarkii, only feeding behaviours (Fig. 4)
were significantly reduced and similar to control period levels when goldfish odours were
introduced (Table 3).
The short-experience and long-experience
A. pallipes, when tested one week after initial training, showed significant reduction of
feeding behaviours (Fig. 4), and time in the
raised posture when goldfish odours were introduced (Table 4). For short-experience A.
pallipes, the time spent in locomotion was
also significantly reduced (Table 4).
Fig. 3. Number of seconds (mean + SE) spent by control animals of (A) Procambarus clarkii and (B) Austropotamobius pallipes in three activities under different
odour treatment conditions. For each behaviour, different letters indicate significant differences between odour
treatments by Tukey tests (P < 0.05).
in feeding movements (Fig. 4) and time in
raised posture were significantly lower than
during food-only periods, but locomotion
time was not altered (Table 3).
Individuals of Austropotamobius pallipes
showed significant reductions in feeding (Fig.
4), locomotion, and raised posture for both
the short-experience and long-experience animals (Table 4). Individuals of both species
and both experience treatments responded to
the goldfish odour as if it represented an elevated predation risk.
Tests One Week After Training.—The shortexperience P. clarkii, when tested one week
Tests Three Weeks After Training.—When
tested three weeks after training, the shortexperience P. clarkii did not show significant
treatment effects for any of the three behaviours based on the Tukey test comparisons
(Table 3). In the case of the long-experience
P. clarkii, individuals showed a very significant reduction in feeding activity (Fig. 4)
upon goldfish introduction, and the decrease
in time in raised posture was almost significant (P = 0.075) (Table 3).
For the short-experience A. pallipes, only
feeding activities (Fig. 4) showed an almost
significant overall treatment effect (ANOVA,
P = 0.070), but there was clearly no difference between food alone and goldfish
odour periods (Fig. 4C). The long-experience
A. pallipes tested three weeks after training
showed no reduction in activities upon goldfish odour introduction (Table 4). Individuals of A. pallipes of both experience treatments had apparently not retained memory of
the learned association by three weeks after
training.
DISCUSSION
The lack of change in the behaviour of control animals when goldfish odour was introduced indicates that individuals of none of
these crayfish species treat goldfish odour as a
stimulus related to predation risk (or anything
else). The absence of a response is reasonable
given the lack of overlap in distribution,
currently and historically, and the herbivorous
nature of goldfish. Following the experience
of goldfish odour and conspecific alarm odour
at the same time, individuals of all four
species showed changes in behaviour fol-
HAZLETT ET AL.: MEMORY CAPABILITIES IN CRAYFISH
445
Fig. 4. Number of seconds (mean + SE) spent in feeding behaviours by individuals of (A) Procambarus clarkii,
short experience, (B) P. clarkii, long experience, (C) Austropotamobius pallipes, short experience and (D) A. pallipes, long experience. Data are presented for the three odour conditions at different times after experiencing the
pairing of goldfish odour and conspecific alarm odour for either two hours (short-experience animals) or 24 hours
(long-experience animals). Different letters indicate significant differences between odour treatments during a given
time since training (Tukey tests, P < 0.05).
lowing the introduction of goldfish odour
alone. The direction of the changes (reduced
levels of feeding, locomotion, and time in the
raised posture) is consistent with the crayfish
treating goldfish odour as a cue associated
with increased predation risk. This pattern of
association is very similar to the results reported for several species of fish (Magurran,
1989; Mathias and Smith, 1993a; Chivers et
al., 1995) and for damselflies (Chivers et al.,
1996). A brief exposure to the two odour
sources together (two hours) was sufficient to
form an association. The learned association
shown by these crayfish should afford some
protection from predation in the field, based
upon the demonstration of a reduction in predation risk by changes in behaviour following the detection of cues associated with elevated predation risk in fish (Mathias and
Smith, 1993b).
In both pairs of species, the invasive
species showed evidence of memory of the
446
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 2, 2002
Table 3. Results from Tukey tests (probability values) comparing the time spent in 3 behaviours (feeding, locomotion,
raised posture) in response to pairs of odour treatments (control vs. food odour, food odour vs. goldfish odour, and
control vs. goldfish odour) by individuals of Procambarus clarkii. Results are presented separately for individuals with
short experience (2 h of pairing of goldfish odour and alarm odour) and long experience (24 h of pairing of goldfish
odour and alarm odour). Results from Tukey tests are reported only for behaviours in which the overall ANOVA showed
a significant difference (P < 0.05).
Short-experience P. clarkii
1 day after training
Feeding
Locomotion
Raised posture
1 week after training
Feeding
Locomotion
Raised posture
3 weeks after training
Feeding
Locomotion
Raised posture
Long-experience P. clarkii
Control-Food
Food-Goldfish
Control-Goldfish
Control-Food
0.001
0.005
0.001
0.001
0.571
0.028
0.437
0.056
0.155
0.001
0.001
0.001
0.001
0.042
0.008
0.398
0.001
0.004
0.001
0.008
0.001
0.001
0.411
0.001
0.876
0.128
0.936
0.001
0.002
0.016
0.015
0.994
0.998
0.245
0.003
0.014
0.142
–
–
0.517
–
–
0.671
–
–
0.001
0.001
0.020
0.001
0.400
0.075
0.002
0.001
0.821
learned association longer than the native
species. Orconectes rusticus showed changes
in food-related behaviour patterns for at least
two weeks after training for both the shortexperience and long-experience animals. In
contrast, the short-experience individuals of
O. virilis showed no indication of a learned
association even one week after training, and
the long-experience O. virilis apparently had
forgotten by two weeks after training. Individuals of Procambarus clarkii had forgotten
the learned association between one and three
weeks after training in the case of the shortexperience animals, but the long-experience
animals still treated goldfish odour as a cue
associated with elevated predation risk three
weeks after training. Individuals of the native
Austropotamobius pallipes, whether trained
for the short or longer period of training, apparently had forgotten by three weeks.
There was an indication in some of the
species that the long-experience animals retained the learned association longer than the
short-experience animals. Short-experience
O. virilis forgot by one week after training,
whereas the long-experience animals of that
species did not appear to forget until two
weeks. The short-experience P. clarkii forgot
between one and three weeks post-training,
whereas the long-experience animals still remembered after three weeks. The other two
species did not show a difference between
length of experience treatments. Longer
memory with more training is of course the
general rule in animals (Dukas 1998).
Food-Goldfish Control-Goldfish
In all four species of crayfish, individuals
exposed to the training situation for just two
hours showed evidence of memory of the
learned association when tested one day later.
The lack of differences among species means
that the hypothesis of invasive species learning faster was not supported by these data.
In many cases, crayfish almost completely
shut down food-related responses upon detection of the learned predation-related cue.
This is in contrast to the results reported earlier (Hazlett, 1999, 2000b) that when
presented with conflicting food and predationrisk cues, crayfish showed intermediate levels of food-related activities but did not cease
feeding completely. That is, while a number
of other crustaceans show a hierarchical organisation in which one cue almost completely dominated the other (Hazlett, 1999,
2000b), crayfish showed a level of activity intermediate to that shown to just one cue or
the other. In the case of all four species used
in this study, very recent exposure to a cue
(one day after training) apparently was strong
enough to result in a hierarchical type of integration of inputs, at least temporarily. Orconectes virilis, one week after training,
showed more of an intermediate pattern of response as was the case for O. virilis tested
with the odour of a natural predator (Hazlett,
1999). Long-experience P. clarkii also
showed an intermediate pattern of activity by
three weeks after training.
These results indicating longer memory of
learned association in invasive species of
HAZLETT ET AL.: MEMORY CAPABILITIES IN CRAYFISH
447
Table 4. Results from Tukey tests (probability values) comparing the time spent in 3 behaviours (feeding, locomotion,
raised posture) in response to pairs of odour treatments (control vs. food odour, food odour vs. goldfish odour, and
control vs. goldfish odour) by individuals of Austropotamobius pallipes. Results are presented separately for individuals
with short experience (2 h of pairing of goldfish odour and alarm odour) and long experience (24 h of pairing of goldfish
odour and alarm odour). Results from Tukey tests are reported only for behaviours in which the overall ANOVA showed
a significant difference (P < 0.05).
Short-experience A. pallipes
1 day after training
Feeding
Locomotion
Raised posture
1 week after training
Feeding
Locomotion
Raised posture
3 weeks after training
Feeding
Locomotion
Raised posture
Long-experience A. pallipes
Control-Food
Food-Goldfish
Control-Goldfish
Control-Food
0.001
0.001
0.002
0.001
0.001
0.041
0.872
0.216
0.423
0.001
0.001
0.001
0.001
0.001
0.001
0.190
0.011
0.008
0.001
0.001
0.003
0.001
0.002
0.002
0.500
0.175
0.968
0.001
0.001
0.003
0.001
0.163
0.027
0.211
0.035
0.600
–
–
–
–
–
–
–
–
–
0.010
–
–
1.000
–
–
0.010
–
–
crayfish as compared to native species are
consistent with other studies of behavioural
plasticity in these categories of animals. Hazlett (2000a) reported that individuals of the
invasive Orconectes rusticus responded more
strongly to heterospecific alarm odours than
did native species of Orconectes which are
being displaced by O. rusticus. Similar results
have been obtained for Procambarus clarkii
and Austropotamobius pallipes (Hazlett et al.,
unpublished). Future tests of the level of behavioural plasticity of species that do well in
new habitats compared to displaced native
species are needed to examine the different
ways animals use information about their environments.
ACKNOWLEDGEMENTS
We acknowledge support from a NATO collaborative
grant (97-6229). We thank Professor Guido Chelazzi for
his hospitality, Aloyzas Burba for his assistance, and
Catherine Bach for comments on the manuscript.
LITERATURE CITED
Blake, M. A., and P. J. B. Hart. 1993. The behavioural
responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels.—Freshwater
Biology 19: 89–97.
Bouwma, P., and B. A. Hazlett. 2001. Integration of multiple predator cues by the crayfish Orconectes propinquus.—Animal Behaviour 61: 771–776.
Capelli, G. M., and B. L. Munjal. 1982. Aggressive interactions and resource competition in relation to
species displacement among crayfish of the genus Orconectes.—Journal of Crustacean Biology 2: 486–492.
Chivers, D. P., G. E. Brown, and R. J. F. Smith. 1995.
Acquired recognition of chemical stimuli from pike,
Esox lucius, by brook stickleback, Culaea inconstans
(Osteichthyes, Gasterosteidae).—Ethology 99: 234–242.
Food-Goldfish Control-Goldfish
———, and R. J. F. Smith. 1994. Fathead minnows,
Pimephales promelas, acquire predator recognition
when alarm substance is associated with the sight of
unfamiliar fish.—Animal Behaviour 48: 597–605.
———, B. D. Wisenden, and R. J. F. Smith. 1996. Damselfly larvae learn to recognize predators from chemical cues in the predator’s diet.—Animal Behaviour 52:
315–320.
Dukas, R. 1998. Constraints on information processing
and their effects on behavior. Pp. 89–127 in R. Dukas,
ed. Cognitive Ecology. Chicago Univ. Press, Chicago.
Garvey, J. E., R. A. Stein, and H. M. Thomas. 1994. Assessing how fish predation and interspecific prey competition influence a crayfish assemblage.—Ecology 75:
532–547.
Gherardi, F., G. N. Baldaccini, P. Ercolini, S. Barbaresi,
G. DeLuise, D. Mazzoni, and M. Mori. 1999. The
situation in Italy. Pp. 107–28 in F. Gherardi and D. M.
Holdich, eds. Crayfish in Europe as Alien Species. How
to Make the Best of a Bad Situation? A. A. Balkema,
Rotterdam.
Hazlett, B. A. 1999. Responses to multiple chemical
cues by the crayfish Orconectes virilis.—Behaviour
136: 161–177.
———. 2000a. Information use by an invading species:
do invaders respond more to alarm odors than native
species?—Biological Invasions 2: 289–294.
———. 2000b. Responses to single and multiple sources
of chemical cues by New Zealand crustaceans.—Journal of Marine and Freshwater Behaviour and Physiology 34: 1–20.
———, and D. R. Schoolmaster. 1998. Responses of
cambarid crayfish to predator odor.—Journal of Chemical Ecology 24: 1757–1770.
Hill, A. M., and D. M. Lodge. 1999. Replacement of resident crayfish by an exotic crayfish: the roles of competition and predation.—Ecological Applications 9:
678–690.
Magurran, A. E. 1989. Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus).—Ethology 82: 216–223.
Mathias, A., D. P. Chivers, and R. J. F. Smith. 1996. Cultural transmission of predator recognition in fishes: in-
448
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 2, 2002
traspecific and interspecific learning.—Animal Behaviour 51: 18–201.
———, and R. J. F. Smith. 1993a. Fathead minnows,
Pimephales promelas, learn to recognize northern pike,
Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike’s diet.—Animal Behaviour 46: 645–656.
———, and ———. 1993b. Chemical alarm signals increase the survival time of fathead minnows
(Pimephales promelas) during encounters with northern pike (Esox lucius).—Behavioral Ecology 4:
260–265.
RECEIVED: 15 March 2001.
ACCEPTED: 4 September 2001.