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