Effects of Predation Risk on Survival, Behaviour and Morphological Traits of Small Juveniles of Concholepas Concholepas (Loco)
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Vol. 472: 169–183, 2013 MARINE ECOLOGY PROGRESS SERIES Published January 9 doi: 10.3354/meps10055 Mar Ecol Prog Ser Effects of predation risk on survival, behaviour and morphological traits of small juveniles of Concholepas concholepas (loco) Patricio H. Manríquez1,*, María Elisa Jara1, Tania Opitz1, Juan Carlos Castilla2, Nelson A. Lagos3 1Instituto de Ciencias Marinas y Limnológicas, Laboratorio Costero de Recursos Acuáticos de Calfuco, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile 2Centro de Conservación Marina, Estación Costera de Investigaciones Marinas. Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114−D, Santiago, Chile 3Centro de Investigación en Ciencias Ambientales, Facultad de Ciencias, Universidad Santo Tomás, Ejercito 146, Chile ABSTRACT: In marine systems, water-borne chemical cues may induce anti-predator responses that influence not only performance and survival of the prey, but also population dynamics and species interaction. The early life stages of marine species with complex life-cycles settle into unpredictable habitats, and therefore may be expected to exploit reliable chemical cues emanat- ing from both prey and predators in order to promote plastic responses to the local conditions. We compared the behavioural responses, survival and growth of early ontogenetic stages of Con - cholepas concholepas exposed to the risk of predation by natural predators that commonly co- occur with it in the intertidal: the crabs Homalaspis plana and Acanthocyclus hassleri and the asteroid Heliaster helianthus. Y-maze experiments indicated that C. concholepas use water-borne cues both to detect prey and deploy strong anti-predator behaviour. Our results indicate lower survival rates of small specimens of C. concholepas when they were maintained in the direct pres- ence of predators rather than under control conditions. Similar results and growth inhibition were found with C. concholepas exposed to seawater in which the predators had been maintained. Quantification of feeding activity and shell thickness in response to predation risk indicated lower prey consumption and thicker shells when C. concholepas were exposed to crab odours compared to control conditions. Our results suggest that this behavioural receptiveness to water-borne cues may be responsible, in part, for the early plasticity of species with complex life-cycles such C. con- cholepas under natural conditions, facilitating predator avoidance and thus enhancing survival. KEY WORDS: Escaping behaviour · Foraging · Growth · Survival · Water-borne cues · Risk-sensitive Resale or republication not permitted without written consent of the publisher INTRODUCTION systems, their adaptive role is not well understood. Prey may respond to predators or damaged con- Predator-prey interactions play an important role specifics by changing physiological, morphological in structuring marine communities (Paine 1966, and behavioural responses (Harvell 1984, 1990, Menge & Lubchenco 1981). Prey selection, predator Appleton & Palmer 1988, Palmer 1990). During early detection and avoidance are essential responses for life stages, meroplanktonic marine species with the survival of any species. However, due to the complex life-cycles disperse and settle into uncer- complexities of trophic relationships in ecological tain benthic habitats, where they must find prey and *Email: [email protected] © Inter-Research 2013 · www.int-res.com 170 Mar Ecol Prog Ser 472: 169–183, 2013 confront local predators. Many of these re sponses ies (Manríquez et al. 2009). Although the presence of are induced by cues or odours emanating from prey and predators can determine the temporal and predators or prey (Lindquist 2002). In general terms, spatial distribution of early settlers of C. concholepas scent and odours emanating from attacked or con- in nature, little information regarding this topic is sumed prey provide the necessary ‘alarm cue’ about available. For instance, the exposure of C. concho - predation risk, and several studies have demon- lepas to effluent from a higher-order predator, the strated that prey can discriminate among risks from subtidal asteroid Meyenaster gelatinosus, alters their different predators and attack strategies (Bourdeau foraging behaviour: juveniles exhibited a reduction 2009). Studies focused on anti-predatory behaviour in foraging time by switching their attention to also report that prey can resolve predator risk due smaller mussels, and larger specimens exposed to to chemical ‘labels’ in the predator diet (Jacobsen & effluent from the same asteroid reduced the number Stabell 2004). Therefore, there is a complex interac- of attacks on mussels (Serra et al. 1997). The 3-way tion between cues emanating from predators and ecological system involving prey (mussels and bar- prey (conspecific and heterospecific), and both can nacles), a keystone predator (C. concholepas), and 2 induce an adequate behavioural response in a prey predators (crabs and asteroid) suggests that settlers species to minimize predation risk (e.g. Alexander & of C. concholepas may show a positive response to Covich 1991). their prey and a negative response to predators The ability of benthic marine invertebrates to re- inhibiting their settlement behaviour. The former is spond to odour cues is widely documented (Castilla supported by the fact that under laboratory condi- 1972, Díaz et al. 1999, Chiussi et al. 2001), and should tions, prey such as small barnacles and mussels be more important in aquatic gastropods that lack induce settlement and metamorphosis in this species visual systems capable of resolving the details of (DiSalvo & Carriker 1994, Manríquez et al. 2004). complex natural seascapes. The predatory marine Moreover, under natural and laboratory conditions, gastropod Concholepas concholepas is an important C. concholepas forages at night and away from component of the intertidal and subtidal communi- refuges (Castilla & Guisado 1979, Dubois et al. 1980), ties along the Pacific coast of South America (Castilla which suggests that foraging in this species is con- 1979). In intertidal habitats, the presence of early set- centrated in periods where there is a low risk of pre- tlers and juveniles of C. concholepas is restricted to dation by visual predators. Furthermore, recent evi- microhabitats dominated by their potential prey such dence suggests that shell colouration in early settlers as mussels and barnacles (Guisado & Castilla 1983, and juveniles of C. concholepas is determined by the Moreno et al. 1993, Manríquez et al. 2009). In these colour of the consumed prey, which, in turn, is an habitats, crabs and starfish are among the potential effective mechanism to reduce visual predation by predators to which C. concholepas are exposed dur- crabs (Manríquez et al. 2009). ing their early ontogeny. The intertidal predatory Although knowledge of the ecological process crabs Acanthocyclus hassleri, A. gayi, Homalaspis influencing post-settlement performance is vital for plana and the asteroid Heliaster helianthus are com- an understanding of marine invertebrates with com- monly found, together with settlers and juveniles of plex life-cycles (Gosselin & Chia 1995), information C. concholepas, inhabiting intertidal and shallow concerning the behavioural responses of early ben- subtidal microhabitats (Paine et al. 1985, Navarrete & thic stages of Concholepas concholepas after settle- Castilla 1988, 1990, Navarrete & Manzur 2008). Sim- ment is almost absent. In aquatic organisms, the ilarly, they coexist with Perumytilus purpuratus mus- response to chemical cues mediates many critical life sel beds and stands of the barnacles Balanus laevis processes with ecological consequences, such as and Notobalanus flosculus, which are common prey prey detection, predator avoidance, reproduction items consumed by C. concholepas (Manríquez et al. and benthic settlement (Lindquist 2002, Webster & 2009). Therefore, in this particular habitat, the be- Weissburg 2009, Bourdeau 2010). Under laboratory havioural responses of C. concholepas to chemical conditions, we tested: (1) if juveniles of C. concho - cues emanating from predators and prey may play an lepas respond differently to odours of different prey; important role in detecting both the appropriate food (2) if these responses to prey are modified in the pres- and the presence of predation risk during their early ence or absence of predator odours; (3) if the pres- ontogeny. ence of predators has negative effects on survival, The potential effect of these cues in modifying the shell thickness and growth of C. concholepas; and (4) performance and survival of small settlers of Con cho - if this response has a negative effect on the feeding lepas concholepas has been the subject of few stud- activity of C. concholepas. Manríquez et al.: Predation risk and early ontogenetic traits in C. concholepas 171 MATERIALS AND METHODS collected from the rocky shore at Calfuco. Specimens of Heliaster helianthus were collected from El Tabo Early settlers (<0.5 cm peristomal length [PL, i.e. (33° 27’ S, central Chile). All experiments were con- the maximum length at the peristomal margin of the ducted between 2005 and 2010 in laboratories at the shell aperture]) and small juveniles (0.6−1.5 cm PL) of Estación Costera de Investigaciones Marinas (ECIM) Concholepas concho lepas were collected from 3 dif- Marine Reserve at Las Cruces and at the Laboratorio ferent rocky shores along the Chilean coast: