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Current Zoology 56 (1): 3642, 2010 Alarm cue induces an antipredator morphological defense in juvenile Nicaragua cichlids Hypsophrys nicaraguensis Maria E. ABATE*, Andrew G. ENG#, Les KAUFMAN Department of Biology, Boston University, Boston, Massachusetts, USA, 02215 Abstract Olfactory cues that indicate predation risk elicit a number of defensive behaviors in fishes, but whether they are sufficient to also induce morphological defenses has received little attention. Cichlids are characterized by a high level of morphological plasticity during development, and the few species that have been tested do exhibit defensive behaviors when exposed to alarm cues released from the damaged skin of conspecifics. We utilized young juvenile Nicaragua cichlids Hypsophrys nicaraguensis to test if the perception of predation risk from alarm cue (conspecific skin extract) alone induces an increased relative body depth which is a defense against gape-limited predators. After two weeks of exposure, siblings that were exposed to conspecific alarm cue increased their relative body depth nearly double the amount of those exposed to distilled water (control) and zebrafish Danio rerio alarm cue. We repeated our measurements over the last two weeks (12 and 14) of cue exposure when the fish were late-stage juveniles to test if the rate of increase was sustained; there were no differences in final dimensions between the three treatments. Our results show that 1) the Nicaragua cichlid has an innate response to conspecific alarm cue which is not a generalized response to an injured fish, and 2) this innate recognition ultimately results in developing a deeper body at a stage of the life history where predation risk is high [Current Zoology 56 (1): 36–42, 2010]. Key words Alarm substance, Inducible defense, Phenotypic plasticity, Cichlid, Chemical cue, Antipredator Predation risk has selected for inducible behavioral, physiological, life history, and morphological defenses that are widespread among the eukaryotes (Tollrian and Harvell, 1999). Chemosensory cues alone are often sufficient to elicit antipredator phenotypic plasticity in individuals across a broad taxonomic distribution of aquatic organisms (Chivers and Smith, 1998; Kats and Dill, 1998). In many instances, olfactory cues can induce morphological plasticity in invertebrates that enhance chance of survival (e.g, Caro et al., 2008; Petrusek et al., 2008). However, to what extent olfactory cues select for antipredator, morphological defenses in fishes remains largely an unanswered question (Chivers et al., 2008). An induced defense provides an individual with a window of opportunity to gauge its predation risk and develop an antipredator response if the benefits outweigh its costs. Antipredator defenses are costly because they pose trade-offs in terms of time and energy (Lima and Dill, 1990; Fraser and Gilliam, 1992; Killen and Brown, 2006), so accurate assessment of risk will ultimately maximize the benefits of the induced defense. Odors that indicate predation risk are not limited to Received Dec. 31, 2009; accepted Jan. 19, 2009 Corresponding author. E-mail: [email protected]. adelphia, Pennsylvania 19104 USA © 2010 Current Zoology # predator scents (Kats and Dill, 1998) or predator dietary cues (Chivers and Mirza, 2001; Brown, 2003). Representatives from many fish families are capable of detecting damage-released alarm substances released at attack (Pfeiffer, 1977; see Mirza et al., 2001) and some fish also respond to disturbance cues released before attack (e.g., Jordao, 2004; Vavrek et al., 2008). These four types of chemical signals are released at different times in relation to the predation event (Wisenden, 2003). Therefore, the potential exists for fish species to utilize the different types of olfactory cues as biological info-chemicals within the context of threat-sensitive predator avoidance (Helfman, 1989). Specifically, dietary or damage-released cues indicate a higher level of risk compared to a predator scent or disturbance cue because they signal a successful strike, so the former should more likely select for induced morphological changes. Damage-released alarm substances are best known for causing vulnerable bystanders to exhibit a short-term fright response which typically includes increased shoal cohesion, area avoidance, dashing, and freezing (Smith, 1999). Since von Frisch’s (1938) happenstance discov- Andrew Eng is now at the Department of Neurosurgery, University of Pennsylvania, Phil- ABATE et al.: Alarm cue induces cichlid morphological defense ery of the fright response induced by the olfactory alarm cue from the skin of an ostariophysan fish, the effects of a number of intrinsic and extrinsic factors on the extent of risk-adverse behavioral responses to fish alarm substances have been tested (e.g., Mirza et al., 2001; Brown, 2003; Leduc et al., 2004; Brown et al., 2006a). However, to our knowledge, there are only three published studies (Stabell and Lwin, 1997; Pollock et al., 2005; Chivers et al., 2008) that specifically tested if a conspecific damage-released alarm cue alone is sufficient to induce a morphological change that could decrease the chance of predation. Of these three, only Pollock et al. (2005) utilized a non-ostariophysan fish, the convict cichlid Archocentrus nigrofasciatus, and they examined the effects of conspecific skin extract on adult morphology. In the current study, we used another Neotropical cichlid, the Nicaragua cichlid Hypsophrys nicaraguensis, to test if morphological changes could be induced by alarm cue at the most vulnerable stage of early development but not persist at a later stage when the costs of the defense should increase. The cichlid propensity for structural plasticity (see West-Eberhard, 2003) which is reversible sometimes (e.g., Meyer, 1990) may facilitate the evolution of an inducible morphological defense that is expressed only when the level of predation risk exceeds the cost of the defense. Although cichlids are Acanthopterygii and do not have the specialized club cells for alarm cue production found in the Ostariophysi (Pfeiffer, 1977), they are good subjects for our study because they do exhibit a fright response in response to conspecific skin extracts For example, convict cichlid adults (e.g., Wisenden and Sargent, 1997), late-stage juveniles (e.g., Foam et al., 2005), and fry still under parental care (Alemadi and Wisenden, 2002) respond to conspecific skin extracts with risk-averse behavior including enhanced homing by individual offspring (Abate and Kaufman, 20061). In previous laboratory studies, the behavioral responses of the Nicaragua cichlid Hypsophrys nicaraguensis to alarm cue and other odorants were similar to those of convict cichlid individuals (Abate, personal observations). In Lake Xiloá, Nicaragua, the Nicaragua cichlid lives in sandy habitats but prefers to breed in rocky habitats (McKaye, 1977). Nicaragua cichlids are substrate brooders that provide bi-parental care and protection for approximately four weeks after the eggs hatch and while the fry become more independent of the nest 1 37 site. Hence as early-stage juveniles move from a protected area, they must rely more on group cohesion and cryptic coloration for protection from predators. A larger body depth in relation to length can decrease fish predation risk by creating a size refuge from attack by gape limited predators, increasing the chance of escape or the predator’s handling costs (e.g., Hambright, 1991; Bronmark et al., 1999). Nicaragua cichlids are streamlined in comparison to the deep-bodied convict cichlid, but adopting a deeper body at an early stage could provide additional protection from small piscivores and larger predaceous conspecific juveniles (Fraser et al., 1993). We further hypothesized that the increase in relative body depth in the Nicaragua cichlid would not be fixed because when the relative costs or benefits of the defense varies during ontogeny, defenses may be restricted to the most vulnerable periods of the life history (e.g., Dannewitz and Petersson, 2001; Ichinose 2002; Vehanen and Hamari, 2004). Particular to a fish increasing relative body depth as it grows is the cost of reduced swimming efficiency due to increased drag (Webb, 1984; Pettersson and Bronmark, 1999; Pettersson and Hedenstrom, 2000). Therefore, at longer lengths, swimming at higher speeds should be more effective than continuing to increase relative body depth to escape a large piscivore. Our experiment was aimed at specifically testing the role of the conspecific alarm substance in eliciting a juvenile gape-limited morphology, so we used a heterospecific chemical alarm cue derived from the allopatric ostariophysan zebrafish Danio rerio as the control for a generalized response to an injured fish odorant. As such, we predicted fish exposed to zebrafish skin extract should not exhibit any morphological changes beyond those in the distilled water treatment. 1 Materials and Methods 1.1 Experimental Setup We obtained young wild Nicaragua cichlids from a reliable aquarium supplier for our brood stock. Ninetyseven juvenile Nicaragua cichlids of a first generation brood were separated from their parents once they reached an early-stage juvenile size [mean standard length (SL) ± SD = 18.11 ± 2.96 mm; total length (TL) = 22.96 ± 3.59 mm; maximum body depth (D) = 4.92 ± 1.12 mm]. They were placed in six 9.5 L experimental aquaria. Each pair of aquaria was assigned a different Abate ME, Kaufman L, 2006. The ontogeny of individual convict cichlid responses to olfactory cues. Ecology and Evolutionary Ethology of Fishes Conference. 38 Current Zoology odor treatment (conspecific skin extract n = 35, distilled water n = 30, or zebrafish skin extract n = 32) for the duration of the experiment. The siblings were evenly distributed so their D, SL, and TL dimensions were equal across all six aquaria (One-Way ANOVAs, P > 0.35) as well as across the assigned treatment tanks (nested One-Way ANOVAs, P > 0.56). The fish were housed in 24°C water under constant filtration, and they were fed commercial flake food twice a day, seven days a week. They were kept on a 12:12 hour light:dark cycle, and the aquarium sides were covered to prevent individuals from receiving visual cues from adjacent tanks. 1.2 Cue Preparation and Delivery Chemical alarm cue treatments were produced from skin fillets taken from Nicaragua cichlids and zebrafish. None of the donor individuals had been previously subjected to alarm cue treatments. The cichlid donors were raised and maintained in similar environments as the test individuals, and the zebrafish donors were raised together in their own aquarium. We used small adult Nicaragua cichlid donors (mean SL = 4.4 cm) because the experimental subjects would be exposed into early adulthood, and preliminary laboratory studies showed that adult skin extracts elicited a fright response in fry, juveniles and adults. For the control for a generalized response to an injured fish odorant, we chose the ostariophysan zebrafish instead of a related non-ostariophysan fish because there is evidence that 1) fish alarm cues are conserved within closely related fish taxa; and 2) the level of antipredator response to the cue declines with increasing phylogenetic distance (Pfeiffer, 1962; Mirza and Chivers, 2001; Kelly et al., 2006). Specifically, Brown et al. (2003) found that juvenile convict cichlids did not exhibit a fright response when exposed to hypoxanthine-3-N-oxide, the putative ostariophysan alarm pheromone, so using the zebrafish cue decreased the chance that the Nicaragua cichlid would associate the odorant with its own risk of predation. Pollock et al. (2005) found the alarm cue from the allopatric nonostariophysan green swordtail Xiphophorus helleri increased foraging behavior in adult convicts. Therefore, using a novel ostariophysan species also reduced the chance that the chemical signal would be misinterpreted as a potential food source and inadvertently affect cichlid foraging behavior and fish growth. Donor fish were euthanized by placing them into a beaker of Alka Seltzer® dissolved in distilled water. Any residual Alka Seltzer was rinsed off with distilled water before filleting. The skin extract was then placed in Vol. 56 No. 1 35 ml of distilled water and homogenized. We removed particulates from the solution by pouring it through polyester aquarium filter floss that had been previously saturated with distilled water. Based on donor fish size, we adjusted the final volume with additional distilled water, so that 1 cm2 of fillet produced 11.4 ml of cue. This concentration elicited fright responses in preliminary laboratory observations and was similar to that used in studies on the convict cichlid (Brown et al., 2004; Foam et al., 2004) and an ostariophysan species (Lawrence and Smith, 1989). Three ml of each treatment cue were dispensed into 13-ml centrifuge tubes and frozen at -20°C. Each treatment aliquot was defrosted completely and mixed with 7 ml of water withdrawn from the target aquarium using a 10-ml pipet prior to delivery. The cue was delivered by pouring the mixture into target aquaria. We prepared and administered aliquots of distilled water in the same fashion for use as our control for treatment delivery. We exposed all the fish to their respective treatments once a day for five days a week. After two weeks, we measured SL, TL and D, and calculated relative body depth (D/SL). We tested if differences between treatments persisted well beyond the young juvenile stage by exposing the fish until they appeared to double in length which coincided with week 12. During those 2.5 months of additional exposure, we concentrated 10 treatment days within the first two weeks of a 21-day cycle. After measuring the body dimensions at the end of week 12, we repeated the two-week odor exposure that the fish had received during the first two weeks of the experiment and took final measurements. 1.3 Statistical Analysis All morphological measurements were LOG10 transformed to meet normality assumptions of ANOVA (two-tailed tests). The statistical software program, JMP Version 5.1 (SAS Institute Inc.), was utilized for data analysis. A one-way ANOVA with aquarium nested within treatment was used to test for differences in body measurements while controlling for variation between the aquaria. The interaction term of a two-way ANOVA with treatment and time as factors tested for a difference in the rate of change over a two-week period. Contrasts were computed to make pair-wise comparisons of slope coefficients (Hartel and Creighton, 2004). 2 Results Siblings exposed to conspecific cue for two weeks grew deeper bodies relative to their length compared to fish in the other two treatments (One-way nested ABATE et al.: Alarm cue induces cichlid morphological defense ANOVA: F2, 91 = 19.31, P < 0.0001; Fig. 1). The interaction term of a two-way ANOVA with Treatment and Time as factors confirmed that the rate of increase in relative body depth was not equal between the treatment groups (F2, 96 = 4.91, P = 0.008). A contrast analysis tested for the difference between slope coefficients and showed that relative body depth increased faster in the conspecific cue treatment than the distilled water control (t = 2.58, P = 0.01) and the zebrafish cue treatment (t = 2.78, P = 0.006). The increase for the fish in the distilled water control was the same as in the zebrafish treatment (t = 0.155, P = 0.88). There were no differences in D, SL, or TL between the treatments (P > 0.2). However, trends in mean D and mean SL changes account for the difference in relative body depth between the conspecific-cue treated fish versus the other two treatments. The smallest percent change in mean SL and largest percent change in mean D occurred in the conspecific cue-treated fish (Fig. 2). Changes in TL follow the same trends as SL. Together the individual’s changes in D and SL in the conspecific cue treatment resulted in a 24% increase in mean relative body depth whereas those of the other two treatments increased by 13%. By week 12 the fish had doubled in length from the beginning of the study with mean SL equal to 34 mm in each of the treatments. When measured at week 12, there was no difference in relative body depth between the three treatments (One-way nested ANOVA: F2, 83 = 0.234, P = 0.79), and variation was reduced even further by the end of week 14 (mean relative body depth = 0.346, 0.35, Fig. 1 Mean relative body depth at zero time and after two weeks of treatment with conspecific or zebrafish alarm cues or distilled water Error bars are 95% confidence intervals. The asterisk indicates a significant difference for both the mean and the slope showing change in relative body depth in the conspecific cue treatment versus the other two treatments. 39 Fig. 2 Percent change in mean standard length, body depth and total length Each percent change in mean determined from [mean at time 0 / (mean at 2 weeks – mean at 0 time) * 100%] in conspecific or zebrafish cue or distilled water treatments. 0.352). Over these last two weeks of the study, the mean changes in linear dimensions were small and ranged from 1% – 4% among all treatments resulting in a 0% – 1% change in mean relative body depth. 3 Discussion Piscivores induce significant behavioral changes including shifts in habitat use and distribution in marine and freshwater ecosystems (Power, 1987; Werner and Hall, 1988; Dahlgren and Eggleston, 2000); and predation selects for differences in morphology between fish populations or generations (e.g., Reznick and Endler, 1982; Reimchen and Nosil, 2002). However, tests for whether fish antipredator morphological defenses arise via developmental plasticity have been limited to only a handful of species (Bronmark and Miner, 1992; Pollock et al., 2005; Eklov and Jonsson, 2007; Januszkiewicz and Robinson, 2007; Chivers et al., 2008). These studies showed that the perception of predation risk induced a deep-bodied morphology, except for Pollock et al. (2005) who found that alarm cues caused reduced growth in adult convict cichlids. Complicating the determination of how taxonomically widespread this phenomenon is in nature is the fact that inducible antipredator morphological responses are often context dependent; that is antipredator tactics and multiple environmental factors influence whether development occurs or not (e.g, Eklov and Jonsson, 2007). It follows that the relative costs and benefits of an induced morphological defense may be much greater for adults than for juveniles in a territorial species like the convict cichlid that has access to shelters. Our study focused on one-month old Nicaragua cichlids when risk of predation should be the highest in 40 Current Zoology this species in order to test whether or not alarm cue alone was sufficient to induce a morphological defense. We found that early-stage juveniles exposed to conspecific alarm cue treatment for two weeks increased their mean relative body depth nearly double that of the fish exposed to distilled water or the zebrafish skin extract. Therefore, as hypothesized this morphological change was in response to a perceived threat to their own species and not a generalized response to an injured fish alarm cue. Although mature males in this species have a larger relative body depth than females, dissection at the end of the experiment revealed that no sexual differentiation had occurred in any of the treatments. In addition, as predicted, the measurements taken when the fish were late-stage juveniles revealed that the conspecific-cue group did not continue to increase in relative body depth. However, the fish exposed to distilled water and zebrafish skin extract reached the same relative body depth as those treated with alarm cue. One possible explanation is that the fish could have recognized in this relatively small living space that their density did not decline, so they may have become sufficiently habituated to the alarm cue after repeated exposure. For example, Brown et al. (2006b) found that juvenile convict cichlids exhibited less antipredator behavior when exposed to conspecific skin extract three times per day versus once a day over three days. The fright response in our study did appear to decrease over time (Abate, personal observations). In addition, visual cues may be essential for maintaining a high-cost antipredator strategy (e.g., Smith and Belk, 2001). In our study, the lack of a visual cue may have indicated that the risk was not high enough to continue increasing body depth even at a slower rate. A second explanation is that although the fish treated with alarm cue after two weeks did not increase in any one dimension more rapidly, the cue induced them to grow into their typical juvenile body shape faster with a relative body depth that is not costly at the maximum size range we examined. Prey individuals with flexible growth patterns may adjust their growth rate to improve their survival (Persson et al., 1996). Changes in growth rate may also correlate with changes in body shape. For example, Vollestad et al. (2004) found that pike cue induced both an increase in crucian carp Carassius carassius relative body depth and growth rate, measured as change in mass. This relationship is the indirect outcome of fish reducing their swimming activity in response to predator cues when food is abundant under Vol. 56 No. 1 laboratory conditions (Johansson and Andersson, 2009) which appears to have played a role in our study as well (Abate, personal observations). In conclusion our experiment shows that the Nicaragua cichlid innately recognizes alarm cue and that cue is sufficient to induce allocation of energy for increasing relative body depth in the youngest juveniles. Our experiment also reveals that cichlid morphological responses to olfactory cues may be transient, and examinations of different stages of the life history will help elucidate their adaptive significance and evolutionary consequences. However, aside from the convict cichlid, we know of only two other species where alarm cue responses have been tested and their examination was restricted to behavior (Barnett, 1982; Jaiswal and Waghray, 1990). Recent attention has been given to the role that predator cues along with selection by food resources may have had on the evolution of the dichotomous fusiform versus deep-bodied ecomorphologies of lacustrine species (e.g., Januszkiewicz and Robinson, 2007). While the photic environment has had significant effects on the diversification of cichlids (e.g., Seehausen, 2008), our study suggests it may be worthwhile to also examine the role of olfactory cues from predation especially in light of the relationship between body shape, diet, and plasticity of the feeding apparatus (Liem and Kaufman, 1984; Wimberger, 1992). The adaptive significance of induced defenses not only enable survival for a species when predation threats vary over time (e.g., Chivers et al., 2008) but may also have facilitated the diversification of fish from a single cichlid population into different ecomorphologies as young fish disperse into new habitats with varying food resources and predation risk. Acknowledgements We thank Hung Pham, Yaejun Lee, Elise Magarian, Nancy Lee, and Kristen Vollrath for their assistance in the laboratory. Financial support was provided by the Undergraduate Research Opportunities Program of Boston University. 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