Biol. Bull. 213: 187-195. (October 2007)
© 2007 Marine Biological Laboratory
Crustacean Social Behavioral Changes in Response to Isolation
Robert Hemsworth,
Wil Villareal,
Blair W. Patullo* and
David L. MacMillan
Department of Zoology, University of Melbourne, Victoria 3010, Australia
* To whom correspondence should be addressed. E-mail: blairp{at}unimelb.edu.au
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Abstract
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Periods of isolation during which animals have no social contact are common in the design of behavioral experiments. They are used, for example, to test memory and recognition responses, or to ensure a baseline condition before experimental manipulations commence. We investigated the effect of isolation periods on the aggressive behavior of matched pairs of the crayfish Cherax destructor in two contexts. The first experiment tested the effects of a period of isolation between two encounters. The second experiment tested the effects of isolation before an encounter by pairing one crayfish from a communal living environment with another crayfish from an isolated one. Fight outcome and aggression levels were analyzed, resulting in three conclusions about the social biology of C. destructor. First, encounters between familiar opponents are influenced by the outcome of the familiarization fight for about 2 weeks. Second, the level of aggression and the outcome of an encounter are affected over different time frames. Third, individuals that are isolated before an encounter can be disadvantaged. These data suggest that isolation, or events that occur during periods of isolation, affect multiple elements of social behavior in C. destructor. This suggestion has implications for the interpretation of previous results and future studies in crustaceans and other taxa.
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Introduction
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There is current interest in social behavior and the factors that affect interactions (e.g., Whitehouse and Lubin, 2005; Hsu et al., 2006; Komdeur, 2006; Sumpter, 2006). Decapod crustaceans are a key subject because investigations of their aggressive behavior permit study of physiological, behavioral, and ecological issues (Breithaupt and Atema, 2000; Perry et al., 2000; Gherardi and Pieraccini, 2004; Figler et al., 2005; Bergman et al., 2006; Edwards and Spitzer, 2006). This is largely because they typically have simple nervous systems and stereotyped aggressive behaviors that have been documented in numerous species (e.g., Bovjerg, 1953; Rubenstein and Hazlett, 1974; Bruski and Dunham, 1987; Huber and Kravitz, 1995). In addition, studies have also tested the effects of serotonin levels on aggression (Yeh et al., 1996; Antonsen and Paul, 1997; Huber et al., 1997), and the effects of psychostimulants (Panksepp and Huber, 2004).
Some of the studies of aggressive behavior examine the social or hierarchy structures that can occur when small groups of animals are housed close together (e.g., Bovbjerg, 1953, 1956; Issa et al., 1999). The ensuing encounters result in winning and losing animals, and the more interactions won the more dominant an animal becomes. These winning and losing outcomes create a history of social experience that can influence future behavior (e.g., Goessmann et al., 2000; Daws et al., 2002; Bergman et al., 2003). Closely associated with the effects of experience is recognition. For a number of crustacean species, victory in contests is determined by dominance status; animals recognize the status of the opponent (e.g., Breithaupt and Atema, 1993; Karavanich and Atema, 1993; Zulandt Schneider et al., 2001; Gherardi and Daniels, 2003). There is also evidence that social behavior around familiar animals is different from behavior around unfamiliar ones, which suggests that some decapods can recognise individuals (e.g., Karavanich and Atema, 1998; Crook et al., 2004; Gherardi and Tiedemann, 2004; Gherardi and Atema, 2005; Detto et al., 2006).
Isolation is an important consideration in experimental design. Investigations often set out to establish a basal level of aggressive activity between pairs of animals by using isolation prior to matched contests. Behavioral changes in rematches represent the influence of prior experience (e.g., Daws et al., 2002; Bergman et al., 2003) or recognition or memory of the prior combatant or its status (e.g., Breithaupt and Atema, 1993; Karavanich and Atema, 1998; Zulandt Schneider et al., 2001). Animals are also usually isolated between matches. When we compared studies of recognition and aggressive behavior in crustaceans, we found substantial variation in how long the effect of previous encounters affects subsequent encounters (5–30 days, Table 1). This variation is interesting because it appears to demonstrate different cognitive abilities between different crustacean species, but it is also potentially problematic because studies use isolation methods that are based on this variable time frame (Table 2).
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Table 1 Examples of the variation in lenth of time that memory or experience affects aggressive behavior in crayfish and other crustaceans
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Few studies test the hypothesis that this period of isolation could itself influence behavior. Some evidence suggests that this is an important consideration in crabs (Courchesne and Barlow, 1971); however, its influence in other groups such as crayfish and lobsters, which are commonly used as behavioral and physiological models (e.g., Yeh et al., 1996; Panksepp and Huber, 2004; Issa and Edwards, 2006), is limited (Rutishauser et al., 2004; Gherardi and Atema, 2005). The matter is pertinent because methodologies vary isolation periods within the same species and also between crustacean groups (Table 3). There are also studies that maintain animals in groups prior to experiments (e.g., Rubenstein and Hazlett, 1974; Winston and Jacobson, 1978; Obermeier and Schmitz, 2003) or in partially isolated groups (e.g., Song et al., 2006—visual and physical isolation but not chemical). Studies on sexual recognition do not seem to isolate animals (e.g., Rufino and Jones, 2001; Díaz and Thiel, 2003), presumably because of the need to establish pair bonds.
We hypothesized that behavior in social interactions of freshwater crayfish, Cherax destructor, would be different after periods of isolation. We targeted two social situations. First we tested the social interactions that occur when there is isolation between encounters. Contests between pairs of crayfish were staged such that each pair had two encounters separated by a period of isolation that was systematically varied. Second we tested whether behavior changed when the isolation occurred before an encounter. For these contests, one encounter was staged for a given pair of crayfish in which one opponent was from a social living environment and the other from an isolated tank where there was no opportunity for social interactions.
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Materials and Methods
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Animals
Crayfish (Cherax destructor Clark) were sourced from a commercial supplier and placed in fiberglass tanks (120 x 50 x 20 cm). The husbandry room was at a constant temperature (18 ± 1 °C) and on a 12 h/12 h light/dark cycle (experiments between 1 and 6 h after the onset of light). Feeding and cleaning occurred weekly, and testing was scheduled the same time after feeding for various treatment groups. About 15–20 crayfish, 3–5 cm carapace length, were kept in each tank and maintained for at least 1 week before experiments. Experimental animals were in good condition with appendages intact. They had not molted within 1 week prior to use, and there was no indication of molting after experimentation. They were matched into pairs that later interacted in staged agonistic encounters.
Pairing crayfish
Carapace and claw length were measured with callipers. Animals from different tanks were randomly chosen and paired primarily on the basis of carapace length and secondarily on claw length. The size variation within each pair was less than 10% carapace length to exclude the possibility that size advantages would affect the outcome of the encounters (Pavey and Fielder, 1996; Daws et al., 2002). Crayfish were individually marked with correction fluid (Pental, Victoria, Australia) on the dorsal carapace before the experiment commenced to distinguish them from one another.
Encounters
The two experiments involved staged encounters between pairs of individuals of C. destructor. These behavioral interactions are common when crayfish and other crustaceans meet (e.g., Gonodactylus festae [Caldwell, 1985]; Homarus americanus [Karavanich and Atema, 1998]; C. destructor [Crook et al., 2004]; Pagurus longicarpus [Gherardi and Tiedemann, 2004]). Contests were staged in glass aquaria (37 x 18 x 22 cm, filled to a depth of 
10 cm with tap water) on a gravel substrate. The external sides of the aquaria were spray painted to exclude external visual stimuli. Each pair was placed into a tank with the opponents separated by a clear barrier. To reduce handling effects, they were given 2–3 min to acclimatize (Baird et al., 2006). The barrier was removed and the pair was allowed to interact for a standard time of 1 h. Tanks were rinsed after each pairing. Encounters were videotaped with a black-and-white CCD camera (Jaycar, Victoria, Australia) connected to a VCR (Panasonic, Victoria, Australia).
Experiments
Isolation between encounters.
To investigate the time frame over which isolation could affect social behavior, we varied the isolation period between bouts of fighting. Three sets of two-round contests were conducted, each involving 20 pairs of size-matched crayfish (Fig. 1A). In the first round, animals in each pair interacted to establish a dominance relationship. They were then returned to their individual tanks. A second round rematched the crayfish after an isolation period of 1, 2, or 3 weeks to determine whether the relationship had changed.
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Figure 1. Experiments manipulated isolation periods between encounters (A), and before encounters (B). Size-matched pairs of Cherax destructor shown with isolation times for the treatment groups in each experiment.
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Isolation before encounters.
To test whether isolation before an encounter affected aggressive behavior, crayfish that had been isolated were matched with opponents that had previous social experience. Animals were divided into two groups: isolates were kept one to a tank (2 liter plastic) and communals were kept in groups of 15 to a tank (fiberglass 120 x 50 x 20 cm). Each isolate animal was matched with one crayfish from a communal tank (n = 20) (Fig. 1B). Four groups of isolates were used: 1, 2, 3, and 4 weeks isolation. To standardize their social experience, communal animals were ordered from the supplier sequentially so that they resided in the husbandry tanks for 1 week prior to pairing.
Observations
Winning and agonistic intensity have been analyzed in several studies on aggressive behavior in crayfish and other crustaceans (e.g., Karavanich and Atema, 1998). We used similar criteria so that our results would be comparable to previous data from a range of crustacean species. The taped footage was analyzed by an observer without knowledge of which treatment was playing. The 1-h encounters produced several contests, or fights. Each contest was defined as a head-on interaction in which the crayfish were within one body length of each other. The initiator, the level of aggression, and the outcome of each fight were recorded. The initiator was the first crayfish to approach an opponent. The level of aggression was calculated as the highest scoring behavior listed in Table 4 during each contest. The loser was the individual that moved more than one body length away from its opponent (Goessmann et al., 2000). For each pair, the numbers of wins and losses from the contests over the 1-h period were tallied, and the crayfish with the most wins was deemed the overall winner of the encounter.
Analysis
Isolation between encounters.
The number of crayfish that won both encounters was tallied for each treatment. If there were no effect of the isolation periods on outcome, either crayfish in the pair would be equally likely to win both encounters irrespective of whether it won in the first round (Zulandt Schneider et al., 2001). Therefore, a chi-square test was used to compare the number of animals that won both encounters, with an expected outcome of 50%. A Yates' correction was applied because there were only two possible outcomes: win in one round or both rounds (Sokal and Rohlf, 1995). The mean aggression levels from the first and second encounters were also compared. If aggression intensity were not influenced by the isolation, levels would remain the same between the two rounds. A paired Student's t-test was used to analyze the difference between the two rounds for each of the three isolation periods. Only the pairs with the same winner in both encounters were included, because a switch in winners would already indicate no effect of isolation.
Isolation before encounters.
Victories of the isolated crayfish were tallied for each period of isolation (1, 2, 3, and 4 weeks). If there were no effect of prior living experience, then the isolated animals should win 50% of the encounters. A Yates' corrected chi-square test was used to compare the number of isolates winning in each of the four groups. There was only one encounter in this experiment, so aggression level was compared between the four treatments using the week 1 group as a comparison point for all other treatments. A one-factor ANOVA (isolation period) tested for an overall difference across the groups, and planned comparisons were applied between the week 1 group and each of the three remaining groups (Quinn and Keough, 2002).
Some crayfish molted or died during the isolation periods, and these were excluded from analysis. However, in all cases we used sample sizes comparable to those in previous crustacean studies (Bergman et al., 2003; Gherardi and Atema, 2005) (final n given in brackets; see Results). Tests were two-sided, with alpha set at 0.05. Data were manipulated in Microsoft Excel (ver. 2000, Microsoft Corporation) and analyzed in Systat (ver. 11, Systat Software Inc.).
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Results
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The encounters followed a general pattern at the start of a trial. After the divider was raised, both opponents showed some exploratory behavior. They slowly walked around the perimeter of the tank and often contacted the glass with their bodies or antennae. Crayfish engaged in multiple fights during the 1-h encounter (median, 8 contest; range, 1 to 29 contests). The duration of each contest was generally less than 5 min but in some cases up to 35 min.
Isolation between encounters
Encounter outcome.
The winner of the first encounter was significantly more likely to win the rematch when the isolation period was 1 or 2 weeks (Fig. 2A). For the week 1 isolation period, the first-round winner won 9 out of 10 round-two encounters (n = 10, 
2 = 4.900, P = 0.027). For the 2-week period, the first-round winners won all of their second encounters (n = 10, 2 = 8.100, P = 0.004). In the 3-week isolation period, the winner of the second round was unpredictable: winners of the first encounter won 8 and lost 3 of the rematches (n = 11, 2 = 1.455, P = 0.228).
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Figure 2. Summary of the effect of isolation between two encounters of matched Cherax destructor. (A) Percentage of crayfish that won both the first and second encounters. More crayfish than predicated by chance won both rounds after 1- and 2-week isolation intervals between the encounters. (B) Mean fight scores for the 2 encounters in each of the 3 treatments. There was a significant decrease in level in the 1-week isolation group. Data from encounters with the same outcome (1 wk: 90% of pairs, n = 9; 2 wk: 100%, n = 10; 3 wk: 73%, n = 8). Error bars +1 SEM. * indicates significance difference P < 0.05, see main text.
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Level of aggression.
There was a significant reduction in aggression levels for crayfish rematched after 1 week of isolation. Eight of 9 winners showed a reduction in fight scores (n = 9, t = 2.578, P = 0.033; Fig. 2B). No difference in aggression was detected between the encounters after 2 and 3 weeks isolation (n = 10, t = 2.124, P = 0.063; n = 8, t = 0.267, P = 0.797).
Isolation before encounters
Encounter outcome.
Crayfish isolated for 1 week won fewer encounters than expected (n = 18, 2 = 4.500, P = 0.034; Fig. 3A). For the 2-, 3-, and 4-week periods, isolated animals won as predicted, with outcomes not differing from 50% (2-wk: n = 10, 2 = 0.100, P = 0.752; 3-wk: n = 18, 2 = 0.056, P = 0.813; 4-wk: n = 11, 2 0.000, P > 0.999; Fig. 3A).
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Figure 3. Summary of the effect of isolation before encounters—opponent from communal living against one from isolated environment. (A) Percentage of isolated crayfish that won. Fewer crayfish than predicted by chance won after being isolated for 1 week. (B) Mean fight scores for the encounters in each of the 4 treatments. There was a significant increase in level between the 1- and 4-week isolation groups. Error bars +1 SEM. * indicates significance difference P < 0.05, see main text.
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Level of aggression.
There was a significant difference in the mean fight scores between the four periods of isolation (F = 4.142, P = 0.010; Fig. 3B). The week 2 and week 3 treatments did not differ from the week 1 period (F1 vs. 2 = 3.719, P1 vs. 2 = 0.059; F1 vs. 3 = 0.373, P1 vs. 3 = 0.544). Fight scores increased in week 4 (F1 vs. 4 = 5.825, P1 vs. 4 = 0.019).
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Discussion
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The staged encounters indicate that two elements of social behavior, outcome and intensity of aggression, are different after periods of isolation when pairs of Cherax destructor fight. The findings demonstrate that fight outcome and intensity can change over different time frames, suggesting that the ability to recognize a conspecific, or the influence of experience on contests, was also altered. Whether individuals were isolated or housed with other crayfish before contests affected the outcome of encounters as well.
Isolation between encounters
When the familiar crayfish were rematched after 1 and 2 weeks of isolation, the behavior of the first encounter prevailed as the determining factor of the outcome in the second round. This indicates that individual recognition, status recognition, the effect of prior experience, or a combination of these processes occurred. These processes are known to exist in C. destructor and other crustaceans (e.g., Karavanich and Atema, 1998; Goessmann et al., 2000; Zulandt Schneider et al., 2001; Breithaupt and Eger, 2002; Daws et al., 2002; Bergman et al., 2003; Crook et al., 2004). This finding suggests that if an individual of C. destructor encountered the same individuals in the wild within short time frames, 1–2 weeks, social standing could be maintained, depending on the amount of additional social activity between encounters.
There was no difference in aggression levels in encounters after the 2- and 3-week isolation periods. In other species, it has been suggested that this is because animals no longer recognize each other (Hojesjo et al., 1998; Herberholz et al., 2001; Zulandt Schneider et al., 2001). The reduction in aggression after 1 week was not detected in the 2-week isolation, but the outcome of the encounters was still significantly biased toward the winner of the first encounter. We conclude from this that the effect of recognition or experience is fading by 2 weeks, and thus multiple behavioral elements—in this case outcome and intensity—can change differently with respect to each other and the duration of the isolation. Reports of fight outcome in Homarus americanus suggest that this may also be the case in another species (experiment F in Karavanich and Atema, 1998).
The outcome of rematched encounters has been investigated in several crustacean species. The research suggests that two main processes govern the behavior in the rematch: experience effects and recognition. It is known that there are short-term effects of winning experience (e.g., 20 min in Orconectes rusticus—Bergman et al., 2003; 24 h in Procambarus clarkii—Daws et al., 2002). Whether our data reflect a winner effect or an experience effect, the effect of the 2-week period of isolation is substantially longer than previously demonstrated in crustaceans. In rematches between familiar pairs of C. destructor after an "experience equalization encounter" to control for status recognition and experience effects, behavioral outcomes were still dictated by the initial familiarization encounter (Crook et al., 2004). This memory of the previous opponent is therefore also likely to explain the outcomes of the contests in our experiment. The possibility of an experience effect cannot, however, be completely discounted.
Isolation before encounters
Isolation affected the winning ability of C. destructor. Short-term isolation (the 1-week period) reduced the number of winning encounters by isolated crayfish. After 3 and 4 weeks, isolates were the overall winners about 50% of the time. This could be interpreted as a return to an unbiased situation in which neither of the two unfamiliar individuals was more likely to win than the other. It suggests that in the wild, short periods of isolation could decrease the probability that a crayfish would win. The amount of serotonin in a crayfish is known to affect retreat behavior (Edwards and Kravitz, 1997; Huber et al., 1997), and it may be that isolation changes the concentration of this neurotransmitter. Alternatively, individuals of C. destructor may need more time to exhibit normal aggressive behavior when placed in isolated environments or different-sized terrain (small containers in this case), because they explore novel surrounds and are affected by complexity in the topography (Basil and Sandeman, 2000; Baird et al., 2006).
Aggression levels differed between the 1- and 4-week isolation groups, suggesting that being isolated in the wild may increase an individual's propensity to invest more energy into its next encounter. This could suggest that the effect of isolation, memory, or experience persists longer than 2 weeks; however, the levels overall were similar (3.5–3.9, Fig. 3B) and at 4 weeks neither crayfish was advantaged in ability to win the fight. Therefore, this difference in aggression level may not be important, because either crayfish could obtain access to resources after the encounter in the wild.
The results appear to indicate an interaction between effects of isolation and communal living. The communal opponents were maintained in groups. There is evidence in other species of crayfish that social structures will form when multiple crayfish are in proximity; however, this has been demonstrated only in small groups (e.g., 4–5 animals, Bovbjerg, 1953; Issa et al., 1999). Our observations in these larger groups suggest that C. destructor will generally not have dominant status because interactions are common and status is therefore reasonably even. If the communal status were a strong factor, then we would have expected the isolates to win more fights because they would be fighting against predominantly submissive animals. This was not the case: isolates won fewer fights in the first week.
Isolation and social behavior
Our results differ from some prior research because they suggest that recognition, experience, or both affect encounters for about 2 weeks. Some studies suggest that less time eliminates the effects of prior experience in some species (Cambarus sp., 1 week [Guiasu and Dunham, 1999]; H. americanus, 1–2 weeks [Karavanich and Atema, 1998]; Orconectes rusticus, 1 week [Zulandt Schneider et al., 2001]; more detail in Table 1). Our results closely resemble unpublished observations cited in Daws et al. (2002) of 2 weeks for P. clarkii. The ecology of the study animals may explain different outcomes in different species. There is no reason to expect all species to be the same in this respect. Three study species are the hermit crab Pagurus longicarpus, the crayfish C. destructor, and the lobster H. americanus. Isolation affects behavior between familiar opponents for 4 days, 2 weeks, and 1–2 weeks for each species, respectively (Gherardi and Atema, 2005; this study; Karavanich and Atema, 1998). P. longicarpus forms aggregations along the shore, and the members remain in proximity, so individuals commonly encounter one another (Gherardi and Atema, 2005) and may have no need to remember opponents for long periods of time. C. destructor and H. americanus, on the other hand, form sparsely populated communities and lead more solitary lives (Karnofsky et al., 1989). They would therefore require longer memory retention because of the need to travel farther and for longer to encounter fellow members. If this type of reasoning is applied, it suggests that different species trade off the need to maintain neighborly contacts according to their environment and lifestyle.
Alternatively, the interpretation of the data may also explain cross-species differences like that previously mentioned between C. destructor, H. americanus, and P. longicarpus. For example, the inference that H. americanus encounters are no longer influenced by prior experience after 1–2 weeks (Karavanich and Atema, 1998) is from data on fight intensity (essentially equivalent to our fight scores). We based our conclusions on intensity and outcome because both could affect C. destructor in the wild. As with other crustaceans, intensity reflects energy investment; outcome reflects access to resources, mates, and territories (e.g., Capelli and Munjal, 1982; Figler et al., 1995, 2005; Issa and Edwards, 2006). Our findings suggest that part of the differences reported in the literature could be due to the amount of social interaction determined by the experimental designs.
There is evidence that isolation influences social behavior of another crustacean, the hermit crab Pagurus samuelis. Isolates win more encounters after they have had no social contact for up to 30 days (Courchesne and Barlow, 1971), which suggests that the influence of isolation may be stronger in C. destructor. We also observed a decrease in the ability to win, as opposed to the increase shown in P. samuelis, so isolation appears to be affecting aggressive behavior differently across species. However, in the hermit crab experiment, the authors pooled data across different isolation periods; we did not in our analysis.
Our results indicate that an animal's social behavior can change as a result of periods of isolation or communal contact with conspecifics. This finding has implications for the design of future studies of the mechanisms involved in recognition and memory. It counsels caution in the use of isolation as a means of establishing a baseline state of physiological or behavioral experiments because the period of isolation can itself be a factor.
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Acknowledgments
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We thank fellow laboratory group members Garry Jolley-Rogers, Kate Naughton, Ying Zheng, Joanne Van der Velden, and Edith Heußlein, as well as the anonymous reviewers, for their ideas and comments on the manuscript. Funding was by an Australian Research Council Discovery Grant to D. Macmillan.
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Footnotes
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Received 22 March 2007; accepted 19 May 2007.
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Abstract
Introduction
