Similarity in Predator-Specific Anti-Predator Behavior In
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Marine Biology (2019) 166:41 https://doi.org/10.1007/s00227-019-3485-5 ORIGINAL PAPER Similarity in predator‑specifc anti‑predator behavior in ecologically distinct limpet species, Scurria viridula (Lottiidae) and Fissurella latimarginata (Fissurellidae) Moisés A. Aguilera1,2 · Monika Weiß3 · Martin Thiel1,2,4 Received: 28 June 2018 / Accepted: 2 February 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Many marine gastropods show species-specifc behavioral responses to diferent predators, but less is known about the mechanisms infuencing diferences or similarities in specifc responses. Herein, we examined whether two limpet species, Scurria viridula (Lamarck, 1819) and Fissurella latimarginata (Sowerby, 1835), show species- and size-specifc similarities or diferences in their reaction to predatory seastars and crabs. Both S. viridula and F. latimarginata reacted to their main seastar predators with escape responses. In contrast, both limpets did not fee from common crab predators, but, instead, fastened to the rock. All tested size classes of both limpet species reacted in a similar way, escaping from seastars, but clamp- ing onto the rock in response to crabs. Limpets could reach velocities sufcient to outrun their specifc seastar predators, but they were not fast enough to escape crabs. Experiments with limpets of diferent shell conditions (with and without shell damage) indicated that F. latimarginata with a damaged shell showed “accommodation movements” (slow movements away from stimulus) in response to predatory crabs. In contrast, intact F. latimarginata and all S. viridula (intact and damaged) clamped the shell down to the substratum. The response details suggest that the keyhole limpet F. latimarginata is more sensitive to predators (faster reaction time, longer escape distances, and higher proportion of reacting individuals) than S. viridula, possibly because the morphology of F. latimarginata (the relationship of its shell size and structure to its total body size) makes this species more vulnerable to predation. Our study suggests that chemically mediated efects of seastar and crab predators result in contrasting behavioral responses of both limpet species, independent of their habitat and morphol- ogy. Despite the diferent characteristics of the limpet species and the identity of predators, the limpets react in comparable ways to similar predator types. Introduction An animal’s ability to assess and react to predator cues Responsible Editor: F. Bulleri. strongly infuences the decision of when and how long/far to escape from predators (Lima and Dill 1990; Lima 1998; Reviewed by P. Camus and A. E. Scherer. Ferrari et al. 2010). These behavioral interactions can have * Martin Thiel important consequences for predator and prey populations, [email protected] and can propagate through the entire food web (e.g., Trussell 1 et al. 2003; Dee et al. 2012; Manzur et al. 2014; Weissburg Departamento de Biología Marina, Facultad Ciencias et al. 2014). Prey organisms often have multiple types of del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile predators, each with unique foraging modes, shape, size, and chemical cues, and consequently, prey respond with an 2 Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile ample range of defensive strategies, each best suited against a particular predator (Turner et al. 2006). When multi- 3 Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, Am Handelshafen 12, ple predators are present simultaneously, conficting prey 27570 Bremerhaven, Germany responses might lead to emergent multiple-predator efects 4 Millennium Nucleus Ecology and Sustainable Management (Sih et al. 1998; Ferrari et al. 2010). Thus, exploring the of Oceanic Island (ESMOI), Coquimbo, Chile suite of prey responses to diferent predators is important Vol.:(0123456789)1 3 41 Page 2 of 13 Marine Biology (2019) 166:41 to understand the mechanisms determining predator–prey Given the diverse suite of predators with diferent forag- dynamics at ecological and evolutionary scales (Lima 1998; ing strategies that gastropods encounter in their natural habi- Pruitt et al. 2012; Brock et al. 2015). tats, some species may adjust their reaction in response to Aquatic invertebrates show a variety of species-specifc diferent predator types, i.e., species with diferent foraging adaptations that minimize the risk of predation. For exam- modes (e.g., Stapley 2004; Turner et al. 2006). In this con- ple, behavioral responses of mollusks to predators can be text, Iwasaki (1993) investigated predator-specifc responses categorized in two major groups, predator avoidance and of the homing limpet Siphonaria sirius which fees from escape (Dalesman et al. 2009). Predator avoidance mini- the whelk Thais clavigera but clamps tightly to its home mizes the risk of encounter with a predator, e.g., when prey scar after encountering the predatory seastar Coscinaste- organisms respond to distant predators (Markowska and rias acutispina (see also Lam 2002). These observations Kidawa 2007). This behavior is common among marine indicate that limpets can perceive predator signals and react gastropods confronted with specifc predators (e.g., Dayton appropriately to predators with diferent foraging strategies. et al. 1977; Rochette and Dill 2000; Powers and Kittinger Changes in shell morphology caused by the previous 2002). The second category of behavioral responses to pred- encounters with predators (e.g., unsuccessful predation by ators, generally referred to as “escape responses” (Kikuchi crabs; West et al. 1991) can alter the behavioral responses of and Dol 1987; San-Martin et al. 2009), reduces the risk of gastropods and their susceptibility to predation. For exam- being preyed upon once an encounter with a predator has ple, some species within the archaeogastropod group are taken place. frequently observed with small pieces broken away from Specifcally, gastropods that encounter predators can their shell. This damage may reduce the efciency of the increase their mucus production (Rochette et al. 1996; Ban- clamp mechanism, because predators could reach the soft cala 2009), show intense shell movements termed “shell body if limpets have a damaged shell margin. Therefore, rocking” or “mushrooming” (Rochette et al. 1999; Espoz and limpets with a damaged shell (i.e., those that experienced a Castilla 2000; Mahon et al. 2002; Markowska and Kidawa previous predator attack) might modify their behavior when 2007), or escape from their predators by rapidly crawling confronted with the same predator type (e.g., crabs), a ques- away (e.g., Iwasaki 1993; Rochette et al. 1996; Lam 2002; tion not previously explored in marine systems. Escobar and Navarrete 2011; Manzur and Navarrete 2011). Limpets from diferent taxa are very common on inter- Some limpets possess “home scars”, where the shell fts tidal and shallow subtidal hard bottoms along the northern- accurately to the underlying substratum, further improving central coast of Chile (e.g., Espoz et al. 2004). Two common the efciency of the clamp mechanism (e.g., Garrity and species, Scurria viridula and Fissurella latimarginata, live Levings 1983; Iwasaki 1993; Williams and Morritt 1995). at diferent zonation levels, intertidal and subtidal, respec- Species from the taxon Scurria (Lindberg 1991) show sig- tively, and, thus, have diferent but equivalent main preda- nifcant diferences in their anti-predator behavior to preda- tors (i.e., seastars and crabs). These limpet species also have tory seastars, moving away from the stimulus in the case of contrasting size, locomotor activity, and morphology, which species without homing behavior, but clamping tightly to the could afect susceptibility and response to diferent preda- rock in the case of species that possess a home scar (Espoz tors: while S. viridula can hide the entire soft body under and Castilla 2000). its shell, the shell of F. latimarginata leaves parts of the Gastropods are susceptible to seastars but also to a wide foot uncovered. In addition, F. latimarginata has a respira- variety of predators that are much more mobile than sea- tory hole on the top of its shell. Thus, these morphological stars such as whelks, fshes, and birds, which may have pro- characteristics may cause a higher vulnerability to predatory found efects on the distribution and abundance of gastro- attacks in F. latimarginata. This could result in signifcant pod populations (e.g., Branch 1985; Mercurio et al. 1985; diferences in anti-predator behavioral responses between Coleman et al. 2004; Navarrete and Manzur 2008; Manzur these two limpet species. et al. 2014). In this context, feld studies about crab–prey In this study, we examined if specifc anti-predator behav- interactions had shown that crab predation is one of the ioral responses of the limpet species vary according to dif- major factors afecting the abundance and distribution of ferent predator types and limpet morphological features. mollusks (e.g., Bertness and Cunningham 1981; Rochette Specifcally, we hypothesized that (a) both S. viridula and and Dill 2000; Grosholz 2005; Wong and Barbeau 2003; F. latimarginata have diferent behavioral responses to dif- Himmelman et al. 2009), and it also played a major role in ferent predator types (i.e., seastars and crabs), and (b) that gastropod shell evolution (Vermeij et al. 1981; West et al. limpets with damaged shells alter anti-predator behavioral 1991; Vermeij 2016). This seems related to the mechanical