Alarm Cue Induces an Antipredator Morphological Defense in Juvenile Nicaragua Cichlids Hypsophrys Nicaraguensis
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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 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