acta ethol (2009) 12:49–53 DOI 10.1007/s10211-009-0054-9
SHORT COMMUNICATION
Differences in aggressive behavior between convict cichlid color morphs: amelanistic convicts lose even with a size advantage Adam R. Reddon & Peter L. Hurd
Received: 24 July 2008 / Revised: 25 December 2008 / Accepted: 9 March 2009 / Published online: 25 March 2009 # Springer-Verlag and ISPA 2009
Abstract Convict cichlids (Archocentrus nigrofasciatus) are a territorial, monogamous, and biparental Central American cichlid fish. Convicts exist in two common color morphs: the wild-type (WT) black-barred form and an amelanistic (AM) barless morph. Color morphs affect aggressive interactions in other species of fish. We staged fights between males of each color morph with varying size asymmetries and found that WT males were able to overcome a size disadvantage by increasing their rate of aggressive behavior. AM males lost more often when smaller than their opponent, apparently because they did not increase their rate of aggressive behavior when at a size disadvantage. We discuss two possible hypotheses to explain these findings: (1) that there are genetic differences in aggressive behavior between the morphs and (2) that AM fish are disadvantaged in staged contests because they are unable to signal via changes in bar coloration. Keywords Color morphs . Aggressive behavior . Dyadic contests . Convict cichlids . Archocentrus nigrofasciatus
Introduction The convict cichlid (Archocentrus nigrofasciatus) is a small freshwater fish found throughout Central America. Convicts are an aggressive and territorial species, forming monoga-
Communicated by E. Goncalves A. R. Reddon : P. L. Hurd (*) Department of Psychology, University of Alberta, Alberta, Canada T6G 2E9 e-mail:
[email protected]
mous pairs during spawning (Wisenden 1995; Barlow 2000). Convict cichlids have proven to be a useful model species in the study of animal behavior. Experiments using convict cichlids have generated important advances in our understanding of mate choice (Santangelo and Itzkowitz 2004), parental care (Richter et al. 2005), and pair bonding (Gumm and Itzkowitz 2007; Bockelman and Itzkowitz 2008). Convict cichlids have been especially valuable in furthering our understanding of aggressive interactions and territoriality (Keeley and Grant 1993a, b; Koops and Grant 1993; Barlow 2000; Draud and Lynch 2002; GagliardiSeeley and Itzkowitz 2006). Size is the key factor in predicting the outcome of staged fights between individual convicts (Koops and Grant 1993) and between sets of breeding pairs (Draud and Lynch 2002). Larger males are also more adept at defending their nest site against intruders (Gagliardi-Seeley and Itzkowitz 2006). Wild-type (WT) convict cichlids possess a series of vertical black bars set atop a white or gray background (Beeching et al. 2002). These markings create the prisoner's garb-like appearance that gives the species its common name. Occasionally, convicts are born with inactive melanophores resulting from homozygous recessive alleles at a single locus (Itzkovich et al. 1981). These fish lack all black, melanin-based coloration, appearing completely white, pink, or orange without the characteristic black bars. These animals are not albinos, but are leucistic, and have no associated abnormalities or deficits. These amelanistic (AM) convicts are rare in the wild (Espmark and Knudsen 2001). Color morphs are a key determinant of fight outcome in many species of fish (Barlow 1983a; Barlow 1983b; Dijkstra and Seehausen 2005). Dijkstra and Seehausen (2005) found that red Pundamilia nyererei had an advantage over a blue-colored sister species P. pundamilia in
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dyadic contests, and this advantage disappeared when special lighting conditions made the color difference imperceptible to the fish. Gold Midas cichlids (Cichlasoma citrinellum) also display an advantage over normally colored individuals by virtue of their coloration and not by genetically coupled aggression (Barlow 1983b). Previous research has suggested that AM and WT convicts do perceive each other as similar but distinct, assortatively mating (Siepen and Crapon de Caprona 1986) and preferentially adopting fry of their own coloration (Espmark and Knudsen 2001). Despite the extensive body of research on the fight behavior of convict cichlids, we know of no studies examining the importance of color morph on aggressive behavior in this species. The object of the current study is to determine if AM and WT convicts differ in their aggressive behavior.
Materials and methods Subjects consisted of 80 adult male convict cichlids, 40 of each color morph. Fish of each morph were purchased at several different times from different local suppliers, originally to serve as size-matched controls for fish in an unrelated study of social influences on sexual differentiation. Subjects ranged in mass from 0.43 to 7.49 g (mean= 2.01±0.179 g). All animals were housed in 95-L, sex- and color morphsegregated, communal aquaria prior to and following experimentation. Aquaria were maintained at 25±1°C on a 12:12-h light/dark cycle. Fish were fed daily on a mixture of prepared flake food and frozen brine shrimp. Forty-eight hours prior to the staged contest, each subject was placed into a private 40-L aquarium and visually isolated from all neighboring aquaria. Each contest was staged between a WT and an AM fish, which were selected at random from the community tanks. The fish were placed in a 115-L aquarium, separated by an opaque Plexiglas divider. After a 90-min acclimation period, the opaque divider was raised. The ensuing contest was video recorded from behind an opaque curtain. Contests were allowed to continue for up to 30 min or until a clear victor emerged. Fights were considered won when the victorious fish vigorously chased the loser around the aquarium three times in succession without any retaliation from the losing animal. Contests that were not decided within 30 min were scored as ties. Duration of tied fights was measured until the occurrence of the last aggressive behavior by either fish. Each animal participated in only one contest. All protocols were approved by the University of Alberta Biological Sciences Animal Policy and Welfare Committee.
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The video recordings of each contest were scored for the number of instances of three different aggressive behaviors in each of the fish. Lateral displays involve the extension of the fin spines along the leading margin of the dorsal and anal fins, followed by the presentation of the broad side of the acting fish to its opponent. Opercular flares (frontal displays) involve the extension of the opercula out to the sides of the fish's head while facing the opponent head on. Biting was defined as physical contact with the opposing fish with the jaws and teeth. Bites were scored any time one fish appeared to make contact between his mouth and the body or fins of his opponent. Mouth-wrestling and circling behaviors also occur in highly escalated fights between convict cichlids. Few of the fights in our experiment reached this level of escalation and these behaviors were not considered in our analysis. Each behavior was scored by instance, individually for each fish. Total instances of each behavior, for each fish, in each fight, were divided by the duration of the fight in minutes to arrive at per minute rates for each behavior. Mass asymmetry was calculated using the following formula: fish mass=ðfish mass þ opponent massÞ ¼ asymmetry score:
Results Of 40 total contests, 22 were won by the WT fish, 11 were won by the AM fish, and seven were undecided after 30 min. Mean fight duration for all fights was 15.7± 1.3 min. On average, winners were heavier than losers (winners=2.12±0.32 g, losers=1.90±0.27 g; paired t=2.11, df=32, p=0.04). Of the 33 decided fights, the AM fish was larger in 19 and the WT fish was larger in ten. The remaining four decided fights were evenly matched to within measurement error (0.1 g). Of the 19 decided fights in which the AM was larger, the AM emerged victorious eight times, with the smaller WT winning 11 times. Of the ten decided fights in which the WT was the larger competitor, nine were successfully won by the WT fish. WT fish are more likely than AM fish to win when larger than their opponents (Yates χ2 =4.38, df=1, p=0.04). This effect was not due to differences in the magnitude of weight asymmetries between these two classes of contests. There was no significant difference between the mass advantage possessed by larger AM fish and larger WT fish (t=1.25, df= 29, p=0.22) in decided fights. A logistic regression of winning strain on the mass asymmetry between the strains revealed that asymmetry between the strains is an effective predictor of fight outcome (z=−1.958, df=32, p=0.05). AM convicts required a 9.43%
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mass advantage to have an equal chance of winning. A log likelihood goodness of fit test indicates that this model generates a significant improvement in model fit over a reduced, intercept-only model (χ2 =4.71, df=1, p=0.03). WT fish that eventually emerged victorious performed more lateral displays (r=−0.45, df=20, p=0.03; Fig. 1c) and bites (r=−0.57, df=20, p=0.01; Fig. 1a), the smaller they were relative to their opponent. WT fish that emerged victorious also appeared to perform more opercular flares, the smaller they were relative to their opponent, but this trend was not significant (r=−0.36, df=20, p=0.10; Fig. 1b). AM fish that eventually went on to win showed no correlation between the frequency of lateral displays and mass asymmetry (r=−0.09, df=9, p=0.79, Fig. 1c). AM winners appeared to use more opercular flares when smaller, but this trend was not significant (r=−0.53, df=9, p=0.10; Fig. 1b). AM winners appeared to bite more, the larger they were relative to the WT fish they defeated, although this trend was also not significant (r=0.57, df=9, p=0.07; Fig. 1a).
Discussion Fight outcome was determined by an interaction between coloration, mass asymmetry, and rates of behavior. WT convict cichlids appeared to be capable of overcoming a size disadvantage against an AM opponent by increasing their frequency of aggressive behaviors. WT fish regularly
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Fig. 1 Per minute aggressive behavior rates as a function of mass asymmetry. WTs (closed circles, solid lines): a winner bites (p=0.01); b winner opercular flares (p=0.10); c winner lateral displays (p= 0.03); d loser bites (p=0.99); e loser opercular flares (p=0.81); and f loser lateral displays (p=0.66). AMs (open circles, dashed lines): a winner bites (p=0.07); b winner opercular flares (p=0.10); c winner
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Loser display rate (lateral displays/min)
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WT fish that lost fights did not show any relationship between the frequency of lateral displays (r=−0.15, df=9, p=0.66; Fig. 1f), opercular flares (r=−0.08, df=9, p=0.81; Fig. 1e), or bites (r=0.002, df=9, p=0.99; Fig. 1d) and the magnitude of the asymmetry between competitors. AM fish that went on to lose tended to lateral display (r=−0.42, df=20, p=0.049; Fig. 1f) and opercular flare (r=−0.48, df=20, p=0.03; Fig. 1e) more, the smaller they were relative to their opponents. There was no relationship between AM loser bite rate and the magnitude of the asymmetry score (r=−0.35, df=20, p=0.11; Fig. 1d).
lateral displays (p=0.79); d loser bites (p=0.11); e loser opercular flares (p=0.03); and f loser lateral displays (p=0.05). Mass asymmetry is calculated as the proportion of the total mass of both fish combined that is held by the target fish. Values greater than 0.5 indicate a fish that is larger than its opponent, and values less than 0.5 indicate a fish that is smaller than its opponent
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defeated larger AM opponents. AM fish did not increase their rate of aggressive behavior when facing larger WT opponents and were mostly incapable of winning against larger WT fish. Tied fights occurred most often when the AM fish was larger (six out of seven cases), suggesting a generalized inability for AM fish to successfully dominate WT fish, even with the benefit of superior size. WT winners tended to bite more, the relatively smaller they were; AM winners, in contrast, show a marginally nonsignificant trend to bite more, the larger they were relative to their opponents. Smaller WT fish may be biting more against larger opponents to compensate for their size disadvantage, whereas AM fish do not use this strategy. The fact that few losing fish ever bit suggests that biting is important in the domination of rivals. This difference in biting may explain the competitive advantage the WT fish held. Lower escalation lateral displays may also be important in WT fish's ability to overcome larger opponents. Although lateral displays show a smaller effect, their use earlier in fights may make them more important in deciding the outcome than behaviors used later in the contest. As with biting behavior, WT winners used more lateral displays the smaller they were relative to their opponent. Winning AM fish, however, did not adjust their lateral display frequency with regard to the mass asymmetry. Strain differences in loser behavior may also account for some of the differences in outcome. WT fish that lost showed no relationship between size asymmetry and any of their aggressive behaviors. AM losers, however, both flared and lateral displayed more the smaller they were, indicating some behavioral resistance to being dominated by a larger fish. Fights in which the WT fish was smaller and yet able to win showed a generally higher level of vigor than any other combination of size advantage and winning strain, emphasizing the importance of aggressive behavior in overcoming an unfavorable size match-up. Why should AM convicts be inferior in dyadic contests? In the Midas cichlid (C. citrinellum), another dimorphic cichlid fish, gold-colored animals possess an inherent advantage in contests against black-barred individuals (Barlow 1983a, b). It is possible that, like in the Midas cichlid, WT convicts have an inherent genetic advantage over AM convicts in contests between the color morphs. In convict cichlids, this advantage may stem from higher overall levels of aggressiveness in the WT morph. Another possibility is that WT fish perceive AM animals as subordinate or unwilling to escalate. Convicts have the ability to rapidly adjust the relative darkness of both the bars and the base coloration (personal observations). Anecdotally, convicts seem to facultatively adjust their coloration depending on social circumstance; for example, dominant or reproducing convicts tend to have much darker bars compared to other individuals from the same cohort
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(personal observations). AM convicts lack active melanophores and have no bar coloration, making it impossible for them to produce signals in this way. Many other fish species signal their aggressive motivation with color changes (Heiligenberg et al. 1972; Beeching 1995; Morris et al. 1995; Hurd 1997; Moretz and Morris 2003) and these signals alter the behavior of the receiving fish (Beeching 1995; Moretz and Morris 2003; Hurd 1997). The behavior of the WT fish may reflect an extreme extension of their natural response to variation in bar coloration. If WT fish perceive the absence of bars on AM animals as a signal of subordinance, they may be willing to escalate against a larger opponent. In this scenario, it is unnecessary for the AM fish to “know” their coloration or behave any differently; only for WT fish to react to them differently that they would to another WT fish. Our results cannot explicitly decouple these two hypotheses, but do clearly illustrate that convict cichlid color morphs differ in aggressive behavior with consequences for fight outcome. Because the convict cichlid is a widely employed species in the study of aggressive behavior, we believe that the demonstrated differences between the color morphs and the potential significance of bar coloration as a signaling apparatus during contest behavior are subjects that merit further research. Acknowledgements We thank Steven Hamblin for his assistance with the analysis. This research was funded by an NSERC discovery grant to PLH. All protocols were approved by the University of Alberta Biological Sciences Animal Policy and Welfare Committee.
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