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 responses, being more susceptible to predation by crabs than efect that crabs exert on gastropod shells because of their undamaged individuals (condition-dependent responses). In anatomy and specifc foraging strategies (e.g., Bertness and addition, we examined whether (c) F. latimarginata, due to Cunningham 1981; Vermeij 2016). its partly unprotected soft body, is more sensitive to predator

1 3 Marine Biology (2019) 166:41 Page 3 of 13 41 cues, exhibiting more marked behavioral responses (e.g., Dayton et al. 1977; Gaymer and Himmelman 2008; Navar- active escape responses over longer distances) to equivalent rete and Manzur 2008). predators (i.e., seastars and crabs) than S. viridula. The mean diameter (± SD) of H. helianthus individuals used herein was 228 mm (± 32 mm) and the mean carapace width of A. gayi was 20.2 mm (± 1.9 mm). The mean diam- Materials and methods eter of M. gelatinosus individuals used in the experiments was 256 mm (± 64 mm), and for H. plana/P. barbiger, the Study sites mean carapace width was 53.4 mm (± 10.8 mm).

Experiments were carried out in rocky inter- and subtidal environments of Coquimbo, Chile (29°57′S; 71°24′W), Experimental design and procedures between January and May 2004. All organisms for the stud- ies of Fissurella latimarginata (Sowerby, 1835) were col- To evaluate anti-predator behaviors of the limpets, we con- lected in Bahía La Herradura (29°58′S; 71°21′W), where ducted both feld and laboratory experiments with similar field studies with this species were also conducted, on treatment designs and procedures. In general, for each lim- subtidal hard bottoms with relatively little direct wave expo- pet species, three predation treatments were considered: (1) sure. Organisms for studies of Scurria viridula (Lamarck, with a seastar, (2) with a crab as predator, and (3) a control 1819) were collected from the intertidal zone of La Pampilla treatment where a direct stimulus with a plastic flamentous (29°57′S; 71°22′W), an exposed rocky shore with intense scouring pad was applied (see Escobar and Navarrete 2011 wave action where feld studies with this species were con- for similar procedure). For the treatment exposure, the shell ducted; seastars Heliaster helianthus (Lamarck, 1816) for of each individual was lightly touched with the respective lab studies with S. viridula were collected in Bahía La predator type (seastar, crab, and scouring pad). Thus, our Herradura. treatment design was similar to that used in the previous studies (Espoz and Castilla 2000, Escobar and Navarrete Study organisms 2011). It should be noted that, because we studied limpet reactions to different predator types, no treatment with The limpets tested for anti-predator responses were Scur- “unstimulated” individuals was included in our experi- ria viridula and Fissurella latimarginata. Scurria viridula ments, since it is not informative in this context (supported occurs in the high-to-low intertidal zone of rocky substrata by the fact that limpets did not react to the scouring pad in exposed and protected areas (Espoz et al. 2004). In con- control—see “Results”). In each treatment (seastar, crab, and trast, F. latimarginata occurs on hard bottoms from the lower control), we measured the reactions of 60 individuals (with intertidal to the shallow subtidal zone (down to 5 m water the exception of F. latimarginata in feld experiments with depth) in sheltered areas with modest wave action (McLean n = 30) of each limpet species. Limpets were subdivided into 1984). While S. viridula is of no commercial interest, F. three size classes (n = 20 individuals per size class; n = 10 latimarginata is subject to an intense artisanal fshery, and individuals per size class in the feld experiments with F. abundances, in particular of large individuals, are compara- latimarginata). Specifcally, the patellid limpets S. viridula tively low. were separated into the following three standard length (SL) Limpet individuals larger than 10 mm shell length, classes: 10–25 mm, 25–35 mm, and 35–55 mm. Each of which were used herein, are usually found on open, bare, the size classes had characteristic shell-color variations, and rock surfaces. We used diferent predator species that are they were considered representative of juveniles, subadults, relatively common in the respective habitat of both lim- and adults (Espoz et al. 2004; Aguilera et al. 2013). Fissurel- pet species. For S. viridula, the seastar Heliaster helian- lid limpets F. latimarginata were divided into the following thus and the crab Acanthocyclus gayi (Milne Edwards and size classes: 20–35 mm, 35–45 mm, and 45–80 mm, repre- Lucas, 1844) (Decapoda: Bellidae) were used as predators, senting juveniles, subadults, and adult individuals (Fernán- and for F. latimarginata, the seastar Meyenaster gelatino- dez et al. 2017). sus (Meyen, 1834) and the xanthid crabs Homalaspis plana The predator stimulus consisted of a touch with one arm (Milne Edwards, 1834) and Paraxanthus barbiger (Poep- (seastar) or chela (crab) of each predator species to each ping, 1836). The latter two crab species have very similar individual limpet. All stimuli were applied with one hand morphology and biology; they occur frequently in the habitat without applying pressure to produce stimuli in a standard of F. latimarginata and were chosen randomly for feld as manner. Each limpet was used only once during the trials. well as for laboratory experiments. Both seastar species are Predator individuals were changed after every fve assays keystone predators in their corresponding habitats accord- (as in Espoz and Castilla 2000), because predators were in ing to feld experiments and diet studies (e.g., Paine 1969; limited supply.

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During each experiment, frst, the original resting posi- F. latimarginata were carried out by scuba diving at water tion of the limpet was carefully marked on the substratum depths of 2–4 m in Bahía La Herradura. without touching the limpet, and then, the stimulus (the respective predator or the scouring pad in the control treat- Specifc details on laboratory experiments ment) was brought in contact with the posterior mantle mar- gin for a maximum of 30 s. If a reaction (moving away from In the laboratory, similar experiments as in the feld were the point of stimulus) occurred within these 30 s, the stimu- conducted under comparable seawater temperature and sub- lus was removed immediately. If no reaction occurred after stratum conditions to reduce environmental variability (e.g., 30 s, the stimulus was removed, and the limpet was observed rock surface structure). Limpets were maintained in separate for at least another 30 s. If no reaction occurred during this predator-free tanks (52 × 102 × 50 cm) and fed (Ulva spp. time, the trial was considered fnished. For limpets that and micro-algae growing on conditioned tiles) for at least reacted within this frst minute, the time interval between 2 days, but not longer than six before being used in labo- the frst contact and frst prey reaction was recorded. Once ratory experiments. Predators were collected 2 days prior the limpet reacted, for S. viridula, we recorded every 30 s to the experiment. All tanks were maintained with running the time that the limpet took to move 1 cm to estimate its seawater and air. Tanks with S. viridula were not flled com- velocity. In experiments with F. latimarginata, at intervals pletely in order to produce an edge with a splash zone, simi- of 30 s, the time that a limpet required to move the distance lar to what these limpets (which live in the high intertidal corresponding to its own shell length was measured. If the zone) experience under natural conditions. velocity dropped to < 1 cm 30 s−1, the reaction was regarded For the experiments with S. viridula, limpets were as fnished. Total duration of the reaction and the distance placed on the seawater-washed cement foor of the labora- moved from the limpets’ original position to the end posi- tory 20 min before the start of experiment. Similar to feld tion were recorded. The maximum observation time after experiments, we considered fat and homogeneous substrata frst predator contact was 5 min. After this time, all limpets to avoid the efects of substratum heterogeneity on limpet stopped moving or at least moved very slowly (e.g., less than movements. For F. latimarginata, individuals were tested 1 cm in 30 min). in a separate tank (52 × 102 × 50 cm) and each limpet was Measurements of limpet shell length were taken after the given an acclimation time of 3 min before the experiment trials. The diferent treatments of the respective experiments was started. The previous assays suggested that this time is were carried out in random order. Only limpets in a resting sufcient for F. latimarginata to reattach to the substratum position were tested. Limpets were considered to be in a rest- or to start moving after manipulation, whereas S. viridula ing position when they were not moving and their whole shell required more time for recovery after manipulation. Com- margin was in contact with the rock in case of S. viridula, or monly Fissurella species tend to react and recover very fast when there was no obvious movement of tentacles or foot in from predator stimuli in the feld compared with other limpet the case of F. latimarginata. Clamping down of the limpet (and chiton) species, a behavior also reported by the other was determined as an individual response in which, after con- authors (e.g., Escobar and Navarrete 2011, Manzur et al. tact with a predator, the limpet sealed its shell to the under- 2014). Some Fissurella species, such as F. crassa, usually lying rock surface (clamp response). Sometimes, a limpet return to normal foraging activities and movement within individual would release some water after sealing the shell. 1–2 min after predator stimuli (touch) (M.A. Aguilera per- sonal observations). In contrast, Scurria limpets tend to take Specifc details on feld experiments > 15 min to acclimate as observed in previous studies (Espoz and Castilla 2000) and in our previous assays. Thus, the Only limpets located on rocky (granite) substratum without acclimation time for the fssurellid was sufcient and did macroalgal or barnacle cover were tested to avoid the unde- not introduce a confounding factor in our experiments. For sired efects of substratum heterogeneity on limpet veloci- this experiment, some tested F. latimarginata individuals ties. Predators for all feld experiments were collected imme- (< 10%) were used twice in replicates (but always with dif- diately prior to the experiments. All feld experiments with ferent predator species), because supply of the keyhole lim- S. viridula in La Pampilla were conducted in the intertidal pet was limited. Limpets that were used twice were allowed zone during low tides early in the morning (no later than 11 2 days to recover before being used with a diferent preda- am). This was done, because both prey and predator were tor species. Preliminary experiments showed that limpets observed to be active mainly during this time of the day (per- reacted similar to untested limpets after this recovery period: sonal observations), when the risk of desiccation is low (see no diferences in behavior were noted between re-used ver- also Barahona and Navarrete 2010 for H. helianthus activ- sus untested limpets, and they reacted as fast as the other ity). Nonetheless, seastar predators can also be active during limpets after contact with seastars or did not react to crab the other tidal stages or time of day. Field experiments with predators after contact.

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Seastar velocities occurred within 60 s, the following variables were recorded: the time between frst contact and reaction, total duration Field experiments were conducted to assess the velocities of the reaction, and the distance the limpet moved from of the respective predators of the two studied limpet spe- its original position. Individuals with an undamaged shell cies for which they showed active escape responses, the sea- (control animals) were tested in the same way. Twenty indi- stars Heliaster helianthus and Meyenaster gelatinosus. We viduals (10 damaged and 10 intact individuals) of medium- measured the velocities of ten individuals of each species. sized S. viridula (33.7 ± 5.8 mm SD shell length) and 40 Each individual was only tested once. Seastars H. helianthus individuals (20 damaged and 20 intact) of medium-sized F. (190.0 ± 11.8 mm SD diameter) were collected during low latimarginata (41.2 ± 6.2 mm) were tested. For S. viridula, tide in the intertidal zone at La Pampilla and immediately we found a few individuals with shell damage, which is why placed on intertidal rock surfaces without any macroalgal the number of replicates was lower than for F. latimarginata, or barnacle cover to avoid interference with substratum which had relatively large numbers of damaged individuals. characteristics. Most seastars started to move after contact Herein, we were only concerned with behavioral diferences with the substratum. 30 s after a seastar started to move, between limpets with intact and damaged shells. Each limpet we measured the time which it required to cover a distance was only tested once and predators were changed after every of 10 cm, equivalent to about half of the body size of each fve limpet trials. The mean carapace width of A. gayi was animal. Velocities of M. gelatinosus (297.8 ± 90.4 mm SD 21.6 (± 2.5) mm and that of H. plana/P. barbiger was 52.6 diameter) were measured in December 2001 at the study site (± 9.8) mm. in Bahía La Herradura. For this species, we used a difer- ent approach to stimulate movement: sea urchins Tetrapygus Statistical analyses niger, which are a common prey organism of M. gelatinosus (Urriago et al. 2011), were placed in the immediate vicinity Independence in the frequency of reacting individuals of of a seastar. Once a seastar started to move towards a sea both limpet species S. viridula and F. latimarginata of dif- urchin, we measured the distance moved by each seastar ferent size classes (small, medium, and large) to diferent within 15–60 s; using the duration and distance of move- predator treatments (seastar, crab, and control) was tested ments, we calculated the velocity for each individual. The with multi-way contingency tables. Thus, we built separate large variation in the size of H. helianthus (refected in a contingency tables for each limpet species, for feld and large standard deviation) used in our study could potentially laboratory trials. Specifcally, we tested if the frequency of afect individual velocities recorded. However, the study by active individuals was independent of treatments (stimulus Barahona and Navarrete (2010) showed that displacement type) and size class. We used one-way ANOVAs to test for of this species is not afected by individual size. Thus, we diferences between limpet size classes for the following assume that size would have only minor or negligible efects response variables: time until reaction, response duration, on individual seastar velocities recorded in the feld (see and escape distances. These analyses were only done for “Results”). experiments with seastars as predators (see “Results”). Normality was tested with a Shapiro–Wilk’s W test, homo- Condition‑dependent prey response: damaged geneity of variances was tested with the Levene test and limpets and crab predators data were log-transformed (Sokal and Rohlf 1981) if they were not normally distributed or the variances did not show A further set of feld experiments was conducted at the same homogeneity (S. viridula, feld and laboratory; escape dis- locations used before (La Pampilla, Bahía La Herradura) to tances). All post hoc tests were conducted with Tukey’s test. investigate condition-dependent diferences in anti-predator Differences in limpet escape velocities between size responses of damaged and undamaged limpets. Preliminary classes (in feld and laboratory experiments) were analyzed observations suggested that damaged individuals modify using a linear mixed-efect model with size and time as fxed their behavior when confronted with crab predators, and that factor and individual replicates as a random factor. Thus, we broken shell margins of limpets were mostly provoked by used a random intercept model (obtained with a maximum- crabs (i.e., by unsuccessful predatory attacks). We selected likelihood estimate), and an autoregressive model of order 1 limpets with a broken shell margin as damaged individuals. (AR1) as the residual autocorrelation structure of velocities Damaged individuals (damaged areas ranged from 0.7 to measured for the diferent replicates through diferent times 12.9 mm2 for S. viridula and from 2.0 to 20.0 mm2 for F. (i.e., velocities were recorded every 30 s; starting from 30 to latimarginata) were selected in the feld and a predatory crab 270 s) (Zuur et al. 2009). This analysis was chosen instead of (again A. gayi for S. viridula and H. plana/P. barbiger for a conventional repeated-measures analysis of variance (RM- F. latimarginata) was brought in contact with the posterior ANOVA), due to decreasing numbers of replicates (subjects) mantle margin for a maximum duration of 30 s. If a reaction during the experiment (i.e., the number of limpets moving

1 3 41 Page 6 of 13 Marine Biology (2019) 166:41 decreased from interval to interval, leading to an unbalanced Table 1 Number of individuals of diferent size classes of (a) Scurria design; Zuur et al. 2009). viridula and (b) Fissurella latimarginata showing active responses (movement away from the point of stimulus), following direct contact To complement the information of ANOVA and mixed with predators and control in feld and laboratory experiments model for response duration, escape distances, and limpet velocities, respectively, we estimated the omega square Treatment Size classes 2 (ω ) efect size for each fxed explanatory variable, which 20–35 mm 35–45 mm 45–80 mm Sum is an unbiased estimator appropriate for small sample sizes a. Scurria viridula (Cohen 1988; Olejnik and Algina 2003). Thus, we used ω2 Field as a measure of variability explained by the independent Seastar 10 13 15 38 variables in our linear models (Olejnik and Algina 2003). Crab 0 0 0 0 We follow the criteria indicated by Kirk (1996) to distin- Control 1 0 2 3 guish large (ω2 ≥ 0.138), medium (ω2 = 0.011–0.059), and Laboratory small (ω2 ≤ 0.010) efect size estimates. All analyses were Seastar 7 11 15 33 conducted in the R environment version 3.5.1 (R Develop- Crab 0 0 0 0 ment Core Team R 2018). Control 0 0 0 0 b. Fissurella latimarginata Results Field Seastar 10 10 10 30 Predator‑specifc limpet responses Crab 0 0 2 2 Control 3 3 2 8 Laboratory In both limpet species, the numbers of responding individu- Seastar 18 17 20 55 als (movement away from the point of stimulus) were higher Crab 3 0 2 5 when confronted with seastar predators than with crabs or Control 0 0 0 0 scouring pad (Table 1a, b). Thus, limpet responses were not independent of the predator type (S. viridula; Field: S. viridula: n = 20; F. latimarginata laboratory: n = 20, feld: n = 10 χ2 = 234.3, P < 0.0001; Lab: χ2 = 135.6, P < 0.0001; F. lati- marginata; Field: χ2 = 69.2, P < 0.0001; Lab: χ2 = 144.9, P < 0.0001). Most S. viridula limpets remained stationary Individuals of Scurria viridula reacted with a slight delay and showed no movement in the controls and in the crab to the seastar stimulus. Both, in the feld and in the labora- treatment, while they showed active escape responses to sea- tory, there were no diferences between the diferent size stars (Table 1a). Similarly, only a few F. latimarginata indi- classes in the time until response (one-way ANOVA; feld: viduals reacted to crab stimuli, while all individuals moved F2,55 = 0.412; P = 0.66; laboratory: F2,55 = 0.546; P = 0.587). away from the seastar (Table 1b). Specifcally, Scurria vir- The total duration of the response (~ 4 min) did not difer idula in crab trials clamped tightly to the underlying rock between the size classes of limpets in the feld experiments surface (clamp response), while they pressed their shell to (one-way ANOVA; F2,55 = 2.014; P = 0.143) and, thus, the rock at the point of stimulus in control trials (i.e., touch- showed a lower efect size (ω2 = 0.034). Meanwhile, the ing shells with scouring pad). In both feld and laboratory, F. laboratory experiments revealed signifcant diferences in latimarginata pressed its shell tightly onto the substratum at response duration between small and intermediate (Tukey’s the point of contact with crabs, while the anterior part of the test = 27. 36; P = 0.020), as well as between small and large shell was lifted and tentacles were brought out and showed S. viridula (Tukey’s test = 43.7; P = 0.018), while there were strong waving movements. no diferences between intermediate and large individuals (Tukey’s test = 16. 33; P = 0.563). The overall efect size for Reaction times, response duration, and distances laboratory experiments was also low (ω2 = 0.031). moved The larger individuals of S. viridula escaped over longer distances than the smaller ones (Fig. 1). Signifcant dif- The escape reactions exhibited by both limpet species in ferences between size classes and medium-to-large efect response to seastars were quite diferent from the short sizes (i.e., ω2 ≥ 0.138) were detected in both field and movements shown in control and/or crab trials. A higher laboratory experiments (field: F2,55 = 4.67; P = 0.0134; 2 2 percentage of limpets responded by moving away in the feld ω = 0.132; lab: F2,55 = 7.72; P = 0.0011; ω = 0.221). In the than in the laboratory experiments, 63.3% in the feld versus feld experiments (Fig. 1a), small S. viridula limpets cov- 55% in the laboratory for S. viridula, and 100% in the feld ered the shortest distance, which was similar to the distance versus 91.7% in the lab for F. latimarginata. covered by the intermediate size class (Mean ± SD; small:

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Fig. 1 Box plot of the dis- tance moved by diferent size classes of the limpets a, b Scurria viridula, and c, d Fis- surella latimarginata, in feld and laboratory experiments. Distances were estimated from the original position to end position after contact with the seastar predators. The black line in each box is the median and the boxes defne the hinge (25% and 75% quartile, and the line is 1.5 times the hinge). Points outside the interval (outliers) are represented as dots. *Sig- nifcant diferences between size classes after one-way ANOVA. P values are reported in the text. Only active individuals (that showed movement away from the predator) were considered for analyses

16.8 ± 11.0 cm; intermediate: 20.1 ± 11.6 cm), but large lim- Similarly, even though, in laboratory experiments, large pets moved signifcantly farther (29.7 ± 13.0 cm) than those limpets covered relatively longer distances than small ones, in the smaller size class (Tukey’s test = 11.5; P = 0.0118). and intermediate size class covered intermediate distances In laboratory experiments (Fig. 1b), the smallest size class (small: 64.2 ± 31.6 cm; intermediate: 83.3 ± 34.0 cm; large: moved a signifcantly shorter distance (10.1 ± 5.0 cm), while 93.5 ± 23.3 cm), no signifcant diferences between size the escape distances of intermediate and large limpets were classes were found (F2,33 = 0.118; P = 0.733 see Fig. 1c). longer and not significantly different (intermediate and Accordingly, the efect size for laboratory experiments was large: 23.5 ± 10.0 cm; Tukey’s test = 8.17; P = 0.1075) (see small (ω2 = − 0.013). Fig. 1b). Fissurella latimarginata always reacted immediately Limpet escape velocities and seastar velocities (within < 2 s) after the frst contact with Meyenaster gela- tinosus. When touched, tentacles were quickly extended For S. viridula, the initial velocity ranged from 0.9 to and limpets showed rapid movements away from the point 1.4 mm s−1 during the frst 30 s, but, thereafter, the velocity of contact. Responses in this species lasted ~ 3 min in the continuously decreased (Fig. 2a, b). Thus, in both feld and feld and ~ 4 min in the laboratory. Both feld and labora- laboratory experiments, we found a signifcant efect of size tory experiments revealed no signifcant diferences in the class and time on velocity recorded (see Table 2a)—large total duration of the response between the diferent size S. viridula moved signifcantly faster than small ones, but classes (Mean ± SD; one-way ANOVA; feld: 185.9 ± 59.9 s; velocities also decreased with time (Fig. 2a, b). In concord- 2 F2,27 = 0.008; P = 0.992; lab: 224.2 ± 58.9 s; F2,33 = 1.05; ance with these results, we found a large (ω = 0.283) and P = 0.312). Accordingly, efect sizes estimated for feld medium (ω2 = 0.050) efect size of size class (fxed efects) and laboratory experiments were small (ω2 = 0.013, and on limpet escape velocities in feld and laboratory experi- ω2 = − 0.071, respectively). ments, respectively. The mean movement distances of the different size The initial escape velocities for F. latimarginata ranged classes of F. latimarginata (see Fig. 1c, d) ranged from from 3.8 to 6.1 mm s−1, which indicates that this species is 53.9 ± 27.6 cm (smallest size class, feld) to 93.5 ± 23.3 cm much faster than S. viridula. Velocities of all size classes (largest size class, lab). Although there was a tendency for of F. latimarginata also continuously decreased over time an increase in movement distance with increasing limpet (Fig. 2c, d), showing a signifcant efect of time and size size (Fig. 1c), no signifcant diferences between size classes classes (Table 2b). Large efect sizes of size classes of F. were detected in field experiments (one-way ANOVA; latimarginata on escape velocities in both feld and labora- 2 2 F2,27 = 2.012; P = 0.153). Shell size of fssurellids had only tory experiments were observed (ω = 0.294 and ω = 0.215, small efects (ω2 = 0.062) on movement distance in the feld. respectively).

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Fig. 2 Scurria viridula, Fis- surella latimarginata. Mean velocities of diferent size classes in feld and laboratory experiments measured at 30-s intervals after the initiation of movement. Error bars indicate SD. Numbers of individuals included in analysis (those escaping from seastars) in parenthesis; the number of individuals showing response decreases continuously dur- ing experiment, because total escape duration of many limpets was < 5 min

Table 2 Results of a linear mixed model for mean velocities of three The measured velocities of the two seastar species were size classes of limpets recorded at diferent times (30–270 s) for (a) quite diferent; velocities of H. helianthus at intertidal levels Scurria viridula Fissurella latimarginata and (b) in feld and labora- ranged from 0.6 to 0.9 mm s−1 (mean 0.7 ± 0.1 mm s−1), tory experiments while velocities of M. gelatinosus were higher, ranging df F P Stdev Residual from 3.8 to 8.3 mm s−1 (and see summary Table 3). Low (a) Scurria viridula individual variation in velocities for H. helianthus and M. Field gelatinosus was observed in the feld (CV = 0.14 and 0.26, Intercept 1 930.6 < 0.0001 0.3482 0.1306 respectively, and see Table 3). Time 8 24.12 < 0.0001 Condition‑dependent prey response: damaged Size 2 35.58 < 0.0001 Time*size 16 0.2872 0.9972 limpets and crab predators Laboratory Intercept 1 912.07 < 0.0001 0.3052 0.1144 None of the 20 feld-tested individuals (10 with natural dam- Time 8 47.26 < 0.0001 age and 10 with intact shells) of S. viridula moved away Size 2 30.73 < 0.0001 from the crab Acanthocyclus gayi when stimulated with this Time*size 16 0.482 0.9547 predator. Damaged and undamaged limpets clamped down (b) Fissurella latimarginata to the rock, while they were in contact with A. gayi, and Field stayed stationary during the experiment. In contrast, feld Intercept 1 695.2 < 0.0001 0.9894 0.3711 experiments with F. latimarginata (n = 20 damaged + 20 Time 8 71.11 < 0.0001 undamaged individuals) revealed diferences in reaction to Size 2 7.812 0.0005 crab stimulus, which depended on the shell damage of a Time*size 16 0.989 0.4691 limpet. Damaged individuals moved away from the stimulus Laboratory more frequently than individuals with intact shells, and thus, Intercept 1 1723.38 < 0.0001 1.1650 0.4368 individual reactions were not independent of shell condition 2 Time 8 89.055 < 0.0001 (df = 1; χ = 12.91; P = 0.0003). Thus, the efect size of shell 2 Size 2 5.123 0.0063 condition on limpet reaction was large (ω = 0.30). Thirteen Time*size 16 2.452 0.0014 of the damaged limpets, but only two of the intact limpets, moved away after predator contact. In general, the movement P Signifcant values ( < 0.05) marked in bold away from predator stimulus for damaged limpets started with a delay of ~ 17 s (16.7 ± 9.2 s) after the crab was with- drawn. The mean duration of the response was 68.8 (± 36.5) s and the mean distance covered was only 10.9 (± 8.0) cm.

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Table 3 Scurria viridula and S. viridula F. latimarginata Fissurella latimarginata: summary of results from feld Field Lab Field Lab and laboratory experiments Seastar Yes Yes Yes Yes Crab No No No No Control No No No No Time until reaction ((sec) ± SD) 10.1 ± 7.9 7.9 ± 7.4 0 0 Duration ((sec) ± SD) 246.8 ± 55.5 223.3 ± 65.2 185.9 ± 58.9 224.2 ± 58.9 Distance ((cm) ± SD) 19.8 ± 11.0 20.7 ± 10.5 66.9 ± 25.5 85.1 ± 42.6 Start velocity ((mm s) ± SD) 1.11 ± 0.48 1.28 ± 0.43 4.76 ± 1.17 4.85 ± 1.76 Velocities seastar predators ((mm H. helianthus M. gelatinosus ­s−1) ± SD) 0.7 ± 0.1 5.2 ± 1.4

Yes movement away from the respective predator, no no movement; time until reaction, duration, distance, start velocity refer to responses to seastar predators only

By contrast, the two intact individuals started their reaction determining specifc anti-predator behavior in the focal lim- after a long delay of 55 s, the escape response lasted only pet species. 35 s, and the distance covered was only about 3 cm.

Limpet behavioral response mechanisms: Discussion chemically versus mechanically mediated

The results of the present study confrmed that the limpet Chemically mediated escape or avoidance responses to species Scurria viridula and Fissurella latimarginata distin- predators have been reported previously in diferent mol- guish between diferent predator types, showing contrasting lusk and sea urchin species in intertidal and subtidal sys- anti-predator behavior to crabs and seastars. These results tems (Dayton et al. 1977; Phillips 1978; Markowska and are well supported by the estimates of the magnitude of Kidawa 2007; Manzur and Navarrete 2011; Urriago et al. predator efects on limpet responses. Moreover, even though 2011; Guderley et al. 2015). Commonly, chemical sub- both limpet species have equivalent responses to predator stances originate from prey or predator species (Dalby et al. types, they showed diferences in the intensity of the active 1987), and their diferent transmission pathways (water/air) escape responses. Likely, these diferences may be due to and chemical properties (Zimmer and Butman 2000) afect diferences in shell morphology with F. latimarginata being prey reactions and behavioral strategies (Mahon et al. 2002; more susceptible to predators than S. viridula, thus reacting Smee and Weissburg 2002; Weissburg et al. 2014). Likely, faster to seastar predators than the latter. Similarly, F. lati- diferential chemical cues from predators (i.e., higher in sea- marginata individuals with damaged shells reacted difer- star and lower in crabs) triggered the specifc and distinct entially to crab predators than intact individuals, suggesting reactions which we observed in our experiments. However, that anti-predator behavior of this limpet is dependent on since we did not evaluate chemical cues, our results only the previous experience (i.e., unsuccessful predator attacks). permit a preliminary interpretation. As indicated by the Active escape responses are an efective strategy of lim- previous studies for some seastar species (e.g., Espoz and pets to reduce predation by seastars (see Dayton et al. 1977; Castilla 2000; Markowska and Kidawa 2007), a treatment Iwasaki 1993; Escobar and Navarrete 2011; Manzur et al. with extracts does not produce anti-predator behavior of the 2014). In contrast, the clamp response after contact with same intensity as direct contact with the living predator (see their respective crab predators is likely to be the most efec- also Manzur and Navarrete 2011). Nonetheless, Mahon et al. tive response to this kind of predator, because limpets are (2002) and Markowska and Kidawa (2007) stated that the unable to escape from fast-moving crabs. In general, both escape behavior of limpets is strongest in response to a com- studied limpet species did not react to control trials, which bination of tactile and chemical stimuli. Our results revealed suggests that a mechanical stimulus is not sufcient to cause that limpets reacted signifcantly more to contact with sea- an active reaction such as an escape response and that anti- stars but not to an inert material (sponge), which supports predator reactions in limpets are mainly induced by chemical this interpretation (see also Escobar and Navarrete 2011). cues (e.g., Rochette et al. 1998; Manzur and Navarrete 2011; However, future studies are required to determine the role Manzur et al. 2014). Here, we discuss the main behavioral and nature of chemical stimuli in mediating both direct and responses observed in our experiments and the mechanism indirect efects on limpet responses (see Manzur et al. 2014).

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Behavioral responses like shell clamping to the substratum viridula (see Table 3). Efects of individual shell size on or shell “rocking” have been described as a relatively efec- escape velocities were large, suggesting that larger limpets tive anti-predator response to seastars for limpets and whelks have a better chance of outrunning seastar predators. High (Rochette et al. 1997, 1999). Ansell (1969) reported that spe- velocities (causing high energetic costs—see Donovan et al. cifc responses are characteristic for certain families of marine 1999) immediately after initiating the escape response ef- mollusks, which may be indicative of a common and presum- ciently reduce the imminent predation risk. Thereafter, we ably ancient origin for these behavioral responses. Espoz observed limpets slowing down and continuing to move at and Castilla (2000) suggested that, within the genus Scurria, slower and supposedly less costly velocities, sufcient to different species showed different anti-predator behavior, get them out of the perceptive range of the predator. This depending on whether they show “homing behavior” and have response is similar to that observed in sea urchins mov- a home scar. Our results show that limpet species without an ing away from seastars (e.g., Manzur and Navarrete 2011; evident home scar like S. viridula and F. latimarginata only Urriago et al. 2011, 2012). In general, the movement path of react with escape to particular predators (seastars), which limpets becomes a random one, and after some time, loco- they might efectively outrun given faster movement veloci- motion ceases (Feder 1963, 1972; this study). Menge (1982) ties than predators recorded in our study (e.g., S. viridula) (see pointed out that efective escape from seastars allows the Table 3). Even though signifcant diferences were found for coexistence of predator and prey in the same habitat (i.e., duration of reaction and escape distances, efect sizes were higher prey movement rate than predator). In this context, it commonly small and so limpet shell size only plays a minor has been found that reaction time and escape distance trave- role in these interactions, which might be more susceptible led by mollusk prey tend to be faster and larger in regions of to health or predator hunger state, substratum characteristics, predator–prey coexistence compared with those outside of or other factors afecting both predator and prey in natural the predator range (see Escobar and Navarrete 2011). Com- conditions. Thus, a hungry seastar might successfully capture parison between limpet and respective seastar velocities of a resting limpet. Both limpet species clamp the shell down both species shows a close correspondence, which means in response to crab predators (with strong mechanical efect), that fast limpets can outrun seastars; on the other hand, it which can easily outrun the limpets. This clamping behavior is possible that a fast seastar individual can catch a slow may also occur in response to the other predators with similar limpet. mechanical stimuli (e.g., fshes for F. latimarginata, and gulls Commonly, seastars are thought to have poor distance for S. viridula), which these limpet species also encounter in perception and appear to be searchers rather than pursu- their natural habitats. Further studies are needed to determine ers (Dayton et al. 1977), which appears to be true for H. if limpet species can also actively avoid and not only escape helianthus but not M. gelatinosus. Heliaster helianthus, from active predators like seastars (Pruitt et al. 2012). which forages during low tide (Tokeshi and Romero 1995), Although both limpet species react in similar ways to sea- moves slowly and randomly during foraging and seems to stars with active predator escape responses, we observed prey on anything crossing its path (Barahona and Navar- strong interspecifc diferences in the reaction time to these rete 2010; Urriago et al. 2011). By contrast, M. gelatinosus predators. The delayed reaction of S. viridula to H. helian- seems to pursue a diferent foraging strategy, because, once thus might be due to the need to verify the potential preda- an encounter with a prey item was initiated, this predator tion risk, as an escape might also bring disadvantages such rapidly initiated a direct pursuit (Dayton et al. 1977). It as desiccation (Williams and Morritt 1995; Miller et al. should be explored, however, if diferent foraging strategies 2009), exposure to other predators, and destabilization (searcher—pursuer) and diferent foraging habitats (i.e., when moving rapidly across the substratum (Geller 1982). intertidal versus subtidal hard bottoms) might lead to the An alternative explanation could be that stimulus transmis- strongly difering velocities of H. helianthus and M. gelati- sion is hampered due to the lack of permanent water fux nosus which we observed (see Table 3). during low tide in the mid-to-higher intertidal zone inhabited by S. viridula. In contrast, F. latimarginata, which inhabits Context‑dependent response of limpets to crab subtidal hard bottoms, reacted without any delay to seastar predators stimuli similar as observed for other subtidal limpets (e.g., Nacella concinna; Markowska and Kidawa 2007). Commonly, stress (i.e., desiccation, hunger levels, and shell damage) results in changes in anti-predator behav- Predator–prey diferences in movement patterns: ior (Formanowicz and Brodie 1988; Vance and Peckarsky seastar–limpet interaction 1997; Ferrari et al. 2010). In our study, we observed that the efect of shell condition on the behavioral response The velocities of all size classes of limpets in most instances to crab predators difered between the two limpet species were slightly faster than seastar velocities, especially for S. and has a large efect on F. latimarginata responses to

1 3 Marine Biology (2019) 166:41 Page 11 of 13 41 predator. Shell damage seems to provoke shifts in limpet Acknowledgements We are most grateful to S. Boltaña and I. Hinojosa responses and might also afect survival. For example, for their help in the feld, and to C. Correa who kindly provided the M. gelatinosus S. viridula velocity data for . Our special thanks go to J. Long, who shell damage may compromise the capacity of gave many helpful comments on an early version of the manuscript. to retain water under their shells, and, thus, may increase This manuscript was substantially improved by numerous constructive the risk of desiccation if they were to move away from a comments from four anonymous reviewers and the editors. We greatly predator in the rocky intertidal zone. Nonetheless, shell appreciate the critical review provided by T. Manzur who commented on the fnal version of the manuscript, and we thank L. Eastman for damage might have only minor negative efects on the editing the English of the fnal manuscript. clamp response, because the large mass of the dorso-ven- tral pedal muscles should still permit S. viridula to cling Author contributions MT and MW conceived the study. MW con- strongly to the substratum (e.g., Cedeño et al. 1996). In ducted the feld and laboratory experiments. MAA reanalyzed all data contrast, the efect of shell damage on F. latimarginata and led the writing of the revised manuscript, which had been initially prepared by MT and MW. appears to be diferent; for example, Cedeño et al. (1996) Fissurella reported that the pedal musculature of species Funding MAA was fnanced by FONDECYT #1160223 and PAI- is less developed than that of patellids. Thus, if the shell CONICYT #79150002, and MT received support through FONDECYT margin is broken, this might be a good point of attack #1161383 during the writing of the manuscript for crabs, and keyhole limpets may not be able to counter these attacks by clamping to the substratum. Consequently, Compliance with ethical standards they might be more vulnerable to crab attacks, making an Conflict of interest “accommodation movement” a more suitable behavior for All authors declare that they have no conficts of interest. survival, particularly as there is no risk of desiccation for the subtidal Fissurella species. Ethical approval All applicable international, national, and/or institu- Natural selection by crab predation can promote the evo- tional guidelines for the care and use of animals were followed. lution of thicker shelled snails (Seeley 1986), but predator- induced phenotypic plasticity may also infuence shell thick- ness (Trussell 1996, Freeman 2007). The need to respond diferentially to crabs (clamp response) and seastars (escape References response) in our predator–prey systems may not only require diferent behaviors, but also results in a trade-of in response Aguilera MA, Valdivia N, Broitman B (2013) Spatial niche diferen- efciency to individual predators. A thick shell permits tiation and coexistence at the edge: co-occurrence distribution efective protection against crab predators (see, e.g., Free- patterms in Scurria limpets. Mar Ecol Prog Ser 483:185–198 Ansell AD (1969) Escape responses of three Indian molluscs. Veliger man 2007), but represents a heavy weight that compromises 12:157–159 escape velocities, while a light shell enables the snail to Bancala F (2009) Function of mucus secretion by lamellose ormer, move fast to outrun seastars, yet making it more suscepti- Haliotis tuberculata lamellosa, in response to starfsh predation. ble to crab predators. In addition, escape reactions might Anim Behav 78:1189–1194 Barahona M, Navarrete S (2010) Movement patterns of the seastar be costly, requiring compensatory mechanisms (e.g., inten- Heliaster helianthus in central Chile: relationship with environ- sifcation of foraging; see Manzur et al. 2014). Therefore, mental conditions and prey availability. Mar Biol 157:647–661 limpets move away only after receiving a strong stimulus Bertness MD, Cunningham C (1981) Crab shell-crushing preda- by seastars and just as fast as necessary to escape from their tion and gastropods architectural defense. J Exp Mar Biol Ecol 50:213–230 seastar predator. The almost instantaneous reaction, faster Branch GM (1985) The impact of predation by kelp gulls Larus domin- escape velocities, longer movement distances, and higher icanus on the sub-antarctic limpet Nacella delesserti. Polar Biol proportion of reacting individuals observed in the keyhole 4:171–177 limpet F. latimarginata (see Table 3) further indicate that Brock KM, Bednekof PA, Paflis P, Foufopoulos P (2015) Evolution of antipredator behavior in an island lizard species, Podarcis erhardii this species is more sensitive to predation risk than the scur- (Reptilia: Lacertidae): the sum of all fears? Evolution 69:216–231 rinid limpet S. viridula. Cedeño J, Voltzow J, Fetcher N (1996) Morphological diferences Despite the diferent characteristics of the limpet spe- between the pedal musculature of patellogastropod and fssurel- cies and the identity of predator species, the limpets react lid limpets. Veliger 39:164–172 Cohen J (1988) Statistical power analysis for the behavioral sciences, in comparable ways to similar predator types. Thus, chemi- Second edn. Lawrence Erlbaum Associated Publishers, Mahwah, cally mediated efects of seastar and crab predators result New Jersey, USA, p 551 in contrasting behavioral responses of both limpet species, Coleman RA, Browne M, Theobald T (2004) Aggregation as defense: independent of the habitat in which they live. These results limpet tenacity changes in response to simulated predator attack. Ecology 85:1153–1159 underline the importance of studying anti-predator responses Dalby JE, Elliot JK, Ross DM (1987) The swim response of the actin- in a multiple-predator context, particularly in prey organisms ian Stomphia didemon to certain asteroids: distributional and phy- that are living in habitats with very diverse predator guilds. logenetic implications. Can J Zool 66:2484–2491

1 3 41 Page 12 of 13 Marine Biology (2019) 166:41

Dalesman S, Rundle SD, Cotton PA (2009) Crawl-out behaviour in Lam KKY (2002) Escape responses of intertidal gastropods on a sub- response to predation cues in an aquatic gastropods: insights from tropical rocky shore in Hong Kong. J Moll Stud 68:297–306 artifcial selection. Evol Ecol 23:907–918 Lima SL (1998) Nonlethal efects in the ecology of predator-prey inter- Dayton PK, Rosenthal RJ, Mahen LC, Antezana T (1977) Population actions. Bioscience 48:25–34 structure and foraging biology of the predaceous Chilean asteroid Lima SL, Dill LM (1990) Behavioral decisions made under the risk Meyenaster gelatinosus and the escape biology of its prey. Mar of predation: a review and prospectus. Can J Zool 68:619–640 Biol 39:361–370 Lindberg DR (1991) Marine biotic interchange between the northern Dee LE, Witman JD, Brandt M (2012) Refugia and top-down control and southern hemispheres. Paleobiology 17:308–324 of the pencil urchin Eucidaris galapaguensis in the Galápagos Mahon AR, Amsler CD, McClintock JB, Baker BJ (2002) Chemo- marine reserve. J Exp Mar Biol Ecol 416–417:135–143 tactile predator avoidance responses of the common Antarctic Donovan D, Baldwin J, Carefoot T (1999) The contribution of anaero- limpet Nacella concinna. Polar Biol 25:469–473 bic energy to gastropod crawling and a re-estimation of minimum Manzur T, Navarrete SA (2011) Scales of detection and escape of the cost of transport in the abalone, Haliotis kamtschatkana (Jonas). sea urchin Tetrapygus niger in interactions with the predatory sun J Exp Mar Biol Ecol 235:273–284 star Heliaster helianthus. J Exp Mar Biol Ecol 407:302–308 Escobar JB, Navarrete SA (2011) Risk recognition and variability in Manzur T, Vidal F, Pantoja JF, Fernández M, Navarrete SA (2014) escape responses among intertidal molluskan grazers to the sun Behavioural and physiological responses of limpet prey to a sea- star Heliaster helianthus. Mar Ecol Prog Ser 421:151–161 star predator and their transmission to basal trophic levels. J Anim Espoz C, Castilla JC (2000) Escape responses of four Chilean intertidal Ecol 83:923–933 limpets to seastars. Mar Biol 137:887–892 Markowska M, Kidawa A (2007) Encounters between Antarctic lim- Espoz C, Lindberg DR, Castilla JC, Simison WB (2004) Los patelogas- pets, Nacella concinna, and predatory sea stars, Lysasterias sp., in trópodos intermareales de Chile y Perú. Rev Chil Hist Nat laboratory and feld experiments. Mar Biol 151:1959–1966 77:257–283 McLean JH (1984) Systematics of Fissurella in the Peruvian and Feder HM (1963) Gastropod defensive responses and their efective- Magallanic Faunal Provinces. Natural History Museum of Los ness in reducing predation by starfshes. Ecology 40:505–512 Angeles County, Los Angeles. Contrib Sci 354:70 Feder HM (1972) Escape responses in marine invertebrates. Sci Am Menge BA (1982) Effects of feeding on the environment: Aster- 227:93–100 oidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Fernández M, Blanco M, Ruano-Chamorro C, Subida MD (2017) Balkema, Rotterdam, pp 521–551 Reproductive output of two benthic resources (Fissurella lati- Mercurio KS, Palmer AR, Lowell RB (1985) Predator-mediated micro- marginata and Loxechinus albus) under different manage- habitat partitioning by two species of visually cryptic, intertidal ment regimes along the coast of central Chile. Lat Am J Aquat limpets. Ecology 66:1417–1425 Res 45:391–402 Miller LP, Harley CDG, Denny MW (2009) The role of temperature Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of and desiccation stress in limiting the local-scale distribution of the predator-prey interactions in aquatic systems: a review and pro- owl limpet, Lottia gigantea. Funct Ecol 23:756–767 spectus. Can J Zool 88:698–724 Navarrete S, Manzur T (2008) Individual- and population-level Formanowicz DR, Brodie ED (1988) Predation risk and forager escape responses of a keystone predator to geographic variation in prey. tactics. Anim Behav 36:1836–1860 Ecology 89:2005–2018 Freeman AS (2007) Specifcity of induced defenses in Mytilus edu- Olejnik S, Algina J (2003) Generalized Eta and Omega squared statis- lis and asymmetrical predator deterrence. Mar Ecol Prog Ser tics. Measures of efect size for some common research designs. 334:145–153 Psychol Methods 8:434–447 Garrity SD, Levings SC (1983) Homing to scars as a defense against Paine RT (1969) The Pisaster—Tegula interaction: prey patches, pred- predators in the pulmonate limpet Siphonaria gigas (Gastropoda). ator food preference and intertidal community structure. Ecology Mar Biol 72:319–324 50:950–961 Gaymer CF, Himmelman JH (2008) A keystone predatory sea star in Phillips DW (1978) Chemical mediation of invertebrate defensive the intertidal zone is controlled by a higher-order predatory sea behaviors and the ability to distinguish between foraging and star in the subtidal zone. Mar Ecol Prog Ser 370:143–153 inactive predators. Mar Biol 49:237–243 Geller JB (1982) Chemically mediated avoidance response of a gastro- Powers SP, Kittinger JN (2002) Hydrodynamic mediation of predator- pod, Tegula funebralis (A. Adams), to a predatory crab Cancer prey interactions: diferential patterns of prey susceptibility and antennarius (Stimpson). J Exp Mar Biol Ecol 65:19–27 predator success explained by variation in water fow. J Exp Mar Grosholz ED (2005) Recent biological invasion may hasten invasional Biol Ecol 273:171–187 meltdown by accelerating historical introductions. Proc Natl Acad Pruitt NJ, Stachowicz JJ, Sih A (2012) Behavioral types of predator Sci USA 102:1088–1091 and prey jointly determine prey survival: potential implications Guderley HE, Himmelman JH, Nadeau M, Cortes HP, Tremblay I, for the maintenance of within-species behavioral variation. Am Janssoone X (2015) Efect of diferent predators on the escape Nat 179:217–227 response of Placopecten magellanicus. Mar Biol 162:1407–1415 R Development Core Team R (2018) R: a language and environment Himmelman JH, Guderley HE, Duncan PF (2009) Responses of the for statistical computing. R Found Stat Comput. http://dx.doi. saucer scallop Amusium balloti to potential predators. J Exp Mar org/10.1007/978-3-540-74686​-7 Biol Ecol 378:58–61 Rochette R, Dill LM (2000) Mortality, behavior and the efects of Iwasaki K (1993) Analyses of limpet defense and predator ofense in predators on the intertidal distribution of littorinid gastropods. J the feld. Mar Biol 116:277–289 Exp Mar Biol Ecol 253:165–191 Kikuchi T, Dol T (1987) Defensive escape response of two trochid Rochette R, McNeil JN, Himmelman JH (1996) Inter- and intra-popu- sand snail species of the genus Umbonium: the efect of species- lation variations in the response of the whelk Buccinum undatum specifc escape response to asteroid predators. Publ Amakusa Mar to the predatory astreroid Leptasterias polaris. Mar Ecol Prog Biol Lab 9:47–65 Ser 142:193–201 Kirk RE (1996) Practical signifcance: a concept whose time has come. Rochette R, Dill LM, Himmelman JH (1997) A feld test of threat sen- Educ Psychol Meas 56:746–759 sitivity in a marine gastropod. Anim Behav 54:1053–1062

1 3 Marine Biology (2019) 166:41 Page 13 of 13 41

Rochette R, Arsenault DJ, Justome B, Himmelmann JH (1998) Chem- helianthus and Meyenaster gelatinosus under feld conditions. J ically-mediated predator-recognition learning in a marine gastro- Exp Mar Biol Ecol 399:17–24 pod. Ecoscience 5:353–360 Urriago JD, Himmelman JH, Gaymer CF (2012) Sea urchin Tetrapygus Rochette R, Maltais M, Dill LM, Himmelman JH (1999) Interpopu- niger distribution on elevated surfaces represents a strategy for lation and context-related diferences in responses of a marine avoiding predatory sea stars. Mar Ecol Prog Ser 444:85–95 gastropod to predation risk. Anim Behav 57:977–987 Vance SA, Peckarsky BL (1997) The efect of mermithid parasitism San-Martin A, Rovirosa J, Gaete K, Olea A, Ampuero J (2009) Mantle on predation of nymphal Baetis bicaudatus (Ephemeroptera) by defensive response of marine pulmonate Trimusculus peruvianus. invertebrates. Oecologia 110:147–152 J Exp Mar Biol Ecol 376:43–47 Vermeij GJ (2016) The limpet form in gastropods: evolution, distribu- Seeley RH (1986) Intense natural selection caused a rapid morphologi- tion and implications for the comparative study of history. Biol J cal transition in a living marine snail. Proc Nat Acad Sci USA Linn Soc 120:22–37 83:6897–6901 Vermeij GJ, Schindel DE, Zipser E (1981) Predation through geo- Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple logical time: evidence from gastropod shell repair. Science predators on prey. Trends Ecol Evol 13:350–355 214:1024–1026 Smee DL, Weissburg MJ (2002) Clamming up: environmental Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of forces diminish the perceptive ability of bivalve prey. Ecology non-consumptive predator efects. Am Nat 184:141–157 87:1587–1598 West K, Cohen A, Baron M (1991) Morphology and behavior of crabs Sokal RR, Rohlf FJ (1981) Biometry. The principles and practice of and gastropods from Lake Tanganyika, Africa: implications for statistics in biological research. W.H. Freeman, San Francisco, lacustrine predator-prey coevolution. Evolution 45:589–607 p 859 Williams GA, Morritt D (1995) Habitat partitioning and thermal tol- Stapley J (2004) Do mountain log skinks (Pseudomoia entrecasteauxii) erance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser modify their behaviour in the presence of two predators? Behav 124:89–103 Ecol Sociobiol 56:185–189 Wong MC, Barbeau MA (2003) Efects of substrate on interactions Tokeshi M, Romero L (1995) Quantitative analysis of foraging behav- between juvenile sea scallops (Placopecten magellanicus Gmelin) iour in a feld population of the South American sun–star Helias- and predatory sea stars (Asterias vulgaris Verrill) and rock crabs ter helianthus. Mar Biol 122:297–303 (Cancer irroratus Say). J Exp Mar Biol Ecol 287:155–178 Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role Zimmer RK, Butman CA (2000) Chemical signaling processes in the of a common crab predator. Evolution 50:448–454 marine environment. Biol Bull 198:168–187 Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated efects Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) in rocky intertidal food chains: predator risk cues alter prey feed- Mixed efects models and extension in ecology with R, 2nd edn. ing rates. Ecology 84:629–640 Springer, New York Turner AM, Turner SE, Lappi HM (2006) Learning, memory and predator avoidance by freshwater snails: efects of experience Publisher’s Note Springer Nature remains neutral with regard to on predator recognition and defensive strategy. Anim Behav jurisdictional claims in published maps and institutional afliations. 72:1443–1450 Urriago JD, Himmelman JH, Gaymer CF (2011) Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster

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