Does the Gathering of Shellfish Affect the Behavior of Gastropod

Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6

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Journal of Experimental Marine Biology and Ecology

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Does the gathering of shellﬁsh affect the behavior of gastropod scavengers on sandy beaches? A ﬁeld experiment

Francisco J. García-García a,⁎, M. José Reyes-Martínez a, M. Carmen Ruiz-Delgado a, Juan E. Sánchez-Moyano b, Macarena Castro Casas c, Alejandro Pérez-Hurtado c a Departamento Sistemas Físicos Químicos y Naturales, Facultad Ciencias Experimentales, Universidad Pablo de Olavide, Carretera de Utrera Km 1, 41013 Sevilla, Spain b Departamento de Zoología, Facultad Biología, Universidad de Sevilla, Av Reina Mercedes 6, 41012 Sevilla, Spain c Departamento de Biología, Facultad Ciencias del Mar y Ambientales, Universidad de Cádiz, Av. Saharahui s/n. 11510 Puerto Real, Cádiz, Spain article info abstract

Article history: Carrion on beaches is an unpredictable and ephemeral resource over time, especially in areas affected by a tidal Received 28 October 2014 regime whereby the ground is frequently washed by incoming tides. In this ecosystem, economic activity, such as Received in revised form 12 February 2015 the commercial harvesting of molluscs, leads to the presence of discarded, damaged and dying specimens of bi- Accepted 24 February 2015 valves on the sand. Thus, although carrion usually represents a minor food source on sandy beaches, human har- Available online xxxx vesting activity can lead to a significant contribution, this being majorly important for scavengers. During low tide, intertidal gastropod scavengers remain buried in the substrate and emerge when they detect carrion. How- Keywords: Behavior ever, in some instances these gastropods may also emerge in response to mechanical disturbance regardless of Cyclope neritea the presence of food. The study reported here aims at investigating the effect of human activity, such as trampling Human trampling on sandy beaches during shellfish gathering, on the behavior of the gastropod scavenger Cyclope neritea in terms Sandy beach of emersion and food locating. This goal was achieved by carrying out short-term field experiments on a sandy Scavenger beach on the European Atlantic coast (SW Spain). The results demonstrate that, as with the presence of carrion on the ground, human trampling affects the behavior of C. neritea, favoring its emersion to the sediment surface and its movement on the ground. It is hypothesized that this is a potential trophic facilitation by shellfishers, since the emersion and movement of gastropods at low tide is induced during the period when the amount of food on the ground increases due to shellfish gathering. Nevertheless, this increased activity also implies a higher predation risk for these scavengers while emerging from the sand. In order to avoid predation, gastropods generally use alarm cues, such as the detection of damaged conspecifics, as an anti-predatory strategy. The behavioral response of C. neritea to the presence of damaged conspecifics was also studied. The results of this study highlight the fact that scavengers emerge from the sediment in response to trampling and the presence of carrion on the sediment surface. Further it is shown that although the presence of damaged conspecifics may act as a cue to gastropods, C. neritea does not respond to this stimulus until it first makes contact. © 2015 Elsevier B.V. All rights reserved.

1. Introduction and populations of the invertebrate communities as a result of the development of trophic interactions (Morton and Britton, 2003; On sandy beaches, carrion is a major food resource for macrofaunal McKillup and McKillup, 1997). One type of positive interaction is trophic beach communities, together with the regular surf phytoplankton and facilitation, a form of commensalism where food material is made more stranded macrophytes (Dugan et al., 2003). Substantial amounts of car- available to one species by the activities of another (Stachowicz, 2001). rion generated by non-predation and predation events supply ecosys- For example, the presence of carrion producers such as birds or humans tems (Beasley et al., 2012; Wilmers et al., 2003). may increase food supply and carrion accessibility for scavenger species The trophic behavior of carrion producers as are some birds, and of (Daleo et al., 2005; Pérez-Hurtado and García, personal observation). human activities such as shellfish gathering, may influence the structure Carrion consumption, provides access to high-quality resources exploited by scavengers, playing an important role in terrestrial and marine ecosystems, thus recent advances in the ecology of food webs em- ⁎ Corresponding author. Tel.: +34 954967359. phasize the importance of scavenging (Barton et al., 2013; Beasley et al., E-mail addresses: [email protected] (F.J. García-García), [email protected] (M. José 2012). Reyes-Martínez), [email protected] (M. Carmen Ruiz-Delgado), [email protected] (J.E. Sánchez-Moyano), [email protected] (M.C. Casas), [email protected] Carrion on beaches can be an unpredictable and ephemeral resource, (A. Pérez-Hurtado). greatly influenced by tidal regimes, where the ground is frequently

http://dx.doi.org/10.1016/j.jembe.2015.02.016 0022-0981/© 2015 Elsevier B.V. All rights reserved. 2 F.J. García-García et al. / Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6 washed by incoming seawater. In this context, carrion location and con- (Southward et al., 1997). This species has a native distribution range sumption can be of major importance, in conjunction with trophic facil- in the Mediterranean Sea, the Black Sea, and along the Atlantic coast itation by humans or birds (McLachlan and Brown, 2006). of the Iberian Peninsula up to the southern part of the Bay of Biscay Carrion deposited on beaches is however also associated with a (northern Spain) (Southward et al., 1997; Sauriau, 1991). Further, the higher predation risk for scavengers emerging from the sand. Therefore, distribution spreads northwards along the French Atlantic coast up to the carrion must be quickly detected and consumed by these scavengers the entrance of the English Channel, this being a probable result of (Morton and Britton, 2003; Morton and Jones, 2003). The use of alarm human-induced introduction (Couceiro et al., 2008; Simon-Bouhet, cues to avoid predation is common in aquatic organisms (Daleo et al., et al., 2006). 2012). For example, the detection of damaged conspecifics by gastropod During low tide C. neritea usually remains buried in the substrate scavengers is frequently used as an anti-predatory strategy (Daleo et al., (Morton, 1960) but it sometimes emerges in response to mechanical 2012; Morton and Britton, 2003; Davenport and Moore, 2002; McKillup disturbance (Bedulli, 1977). In this sense, the observations of Bedulli and McKillup, 1994; Stenzler and Atema, 1977). (1977) could serve as a basis for the hypothesis that the effect of The effect of trampling on shores has been extensively studied human trampling on the sediment stimulates the activity of the snail, (e.g., Farris et al., 2013; Davenport and Davenport, 2006; Beauchamp which could in turn lead it to detect food faster. S. marginatus and and Gowing, 1982) and it is associated with economic activities such C. neritea co-occur on sandy beaches in Southern Spain, and the bivalves as tourism and commercial harvesting in coastal areas (Sarmento and discarded by shellfishermen are a potential source of food for the Santos, 2012; Schlacher and Thompson, 2012; Veloso et al., 2008). It gastropod. has been reported in literature that human trampling and shellfish har- In this context, by using C. neritea as an experimental subject, the vesting, clearly have negative effects on the fauna of sandy beaches work reported here aims at describing the responses of a gastropod (e.g., Farris et al., 2013; Sheehan et al., 2010; Moffett et al., 1998) and scavenger to the presence of human trampling, food, and damaged con- this is considered to be a major cause of biodiversity loss in protected geners during low tides on a sandy beach. On considering the goals of areas (Andersen, 1995). this study the following questions were raised: Although there are no published studies to date regarding the re- Is there a change in the behavior of C. neritea as a result of stimuli sponses of scavengers to human trampling, it is possible that these ani- caused by trampling by shellfishermen and due to the presence of mals find and consume carrion faster when stimulated. In this sense, a carrion? trophic facilitation effect may be hypothesized, whereby an increase in Does the presence of damaged congeners inhibit the approach of the activity of gastropods caused by trampling allows these organisms C. neritea to the prey, this being as a defensive response to reduce the to find the carrion faster than when they are buried and inactive in risk of predation? the sediment. In Southern Europe, the bivalve Solen marginatus, the grooved razor 2. Materials and methods clam, is a commercial species that burrows in the soft bottom. This species is exploited in natural beds in intertidal and shallow subtidal areas 2.1. Study area of estuaries and beaches. Over the years, and especially during the spring and summer months, this area is harvested intensively. The re- Field experiments were carried out at Levante beach during spring moval techniques that are frequently used cause injury to the bodies tides from April to May of 2013. Levante beach is 4.2 km long and is a of the clams and, as a consequence, specimens are left on the sand as protected site within the Cadiz Bay Natural Park, located in southern carrion. In addition, shellfish gatherers tend to leave damaged grooved Spain (36°32′58″ N, 6°13′35″ W). This is a dissipative beach that has a razors that are smaller than the required commercial sizes on the mesotidal regime (with a tidal amplitude up to 3.2 m) with up to sand, as potential carrion for scavengers (Pérez-Hurtado and García, 150 m of beach uncovered during spring tides. To the east, this site is personal observations) (Fig. 1). bordered by a densely urbanized site (Valdelagrana) and to the west The nassariid Cyclope neritea is a burrowing marine snail that is is the mouth of the San Pedro River. Behind the beach is also the pres- found in shallow and intertidal habitats with medium to fine sand. ence of native vegetation, dunes, and a salt marsh. During the study pe- This species has dense populations in areas of the Levante beach, riod the air temperature at Levante beach ranged from 19.9 to 21.6 °C, where S. marginatus harvesting is an intense activity. Like other the ground temperature ranged from 17.6 to 20.7 °C, and the interstitial nassariids, C. neritea is predominantly a scavenger (Bachelet et al., water had a salinity of 36. 2004), although it also ingests a mixture of sand, bacteria and diatoms The area in which the experiments were carried out was selected due to the abundance of C. neritea and the intensity of S. marginatus harvesting. In addition, the distance to the line of low tide meant that the plots were exposed while the experiments were carried out. At this site, located approximately 140 m from the lower level of the tide, there is an abundant population of the snail C. neritea, reaching a maxi- mum of 40 specimens/m2 and an average of 16 specimens/m2 (personal observation). Throughout the year, and especially during the spring and summer months, the area is harvested intensively by around 20 shellfishermen collecting grooved razor clams (S. marginatus). Shellfishermen spend an average of two and half hours at low tide collecting an average of 10 kg of razor clams per person, with a total of around 200 kg of bivalves collected per day. Approximately 10–15% of the catch is damaged during harvesting. Thus, some 20–25 kg of crushed razor clams are discarded of which around 44% is preyed by snails (Pérez-Hurtado and García, personal observation).

2.2. Effect of human trampling on the activity of C. neritea

The influence of the disturbance caused by human trampling during Fig. 1. Cyclope neritea on carrion of Solen marginatus. low tide on the activity of C. neritea was assessed by marking out 24 F.J. García-García et al. / Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6 3 plots of 1 m2 on the mid-tide zone parallel to the coastline. Plots were of variances (Levene test). Homogeneous groups for among-subject fac- allocated in two groups of 12 plots each. Plots were set 2 m apart in tors were separated by a Student–Newman–Keuls (SNK) test, while order to avoid interference. During the experiment, one group of plots within-subject factors were separated by the Bonferroni test. In the remained undisturbed, while the remaining 12 were subjected to dis- case of significant interactions, multiple comparisons between factors turbance, which involved walking for 3 min on the plots prior to were made by the Bonferroni test. In the experiment on the effect of counting the C. neritea specimens on the surface. Trampling started trampling on C. neritea activity, a t-test was applied to determine 5 min before each census (during the 2 min prior to the census the whether the mean abundance values in each treatment differed signifi- plots were kept undisturbed in order to avoid the burial of gastropods cantly between ebbing and flooding time. Statistical analyses were con- caused by trampling); and was conducted by people of similar body ducted with the PASW Statistics 18 software. mass (about 70 kg) at a frequency of 50 steps per minute (similar to that produced by shellfish gatherers as they move in search of bivalves; 3. Results Pérez-Hurtado and García, personal observation). The snails located on the surface of each plot were counted every 15 min. In order to avoid 3.1. Effect of human trampling on the activity of C. neritea disturbance on the plots caused by the movement of researchers during the censuses, counts were performed from a distance of at least 1 m Trampled and undisturbed plots differed, significantly in the number from the edge of each plot. Because the proximity of the water could af- of snails, (F(1,24) = 216.55; p b 0.0001) throughout the sampling period fect the ability of the snails to emerge or retract in the sand (Morton and (F(7.6,24) =8.4;pb 0.0001) with an interaction between the two factors Jones, 2003; Kitching et al., 1987) and in order to separate the effects of (F(7.6,24) = 4.45; p b 0.0001) (Table 1, Fig. 2). The results of the tidal fluctuations on the experiment, the distance between the low Bonferroni test show that the mean number of specimens found was water mark and the plots was measured as each census was carried significantly higher in trampled plots than in undisturbed ones out. The counts were made while the tide was ebbing and flooding, (p b 0.001), except at the end of the experimental period during and the experiment was ended when the plots were covered by incom- flooding. Furthermore, the number of C. neritea that emerged onto the ing water. surface in trampled plots varied depending on the tidal cycle. The abundance values in these plots were significantly higher during ebbing than 2.3. Influence of trampling and the presence of food on C. neritea activity during flooding (t = 3.65; p b 0.01). Nevertheless, differences were not observed between the undisturbed plots during the experiment, except In an effort to determine whether the presence of food affects the re- when the water had reached the plots (t = −0.47, p N 0.05), in which sponse of C. neritea to trampling, an experimental design similar to case the snails emerged to the surface regardless of the treatment that outlined above was repeated but with the presence of food (disturbed and undisturbed). (S. marginatus carrion) as an additional factor. In this case, 24 plots of 1m2 were laid out: 12 plots were perturbed by trampling, as in the pre- 3.2. Influence of trampling and the presence of food on C. neritea activity vious experiment, and 12 were left undisturbed. For each treatment, 6 pieces of razor clam (ca. 5 g each) were randomly deposited on 6 A small number of individuals were observed in the plots without plots just before starting the experiment. During trampling, care was food, while plots with added carrion had a higher number of C. neritea taken to avoid stepping on food samples, in order to avoid burial. Cen- specimens on the surface (Fig. 3). The undisturbed control plots, in suses were repeated every 15 min for 2 h. which food was not provided, contained the lowest number of specimens. Significant differences were observed between disturbance treat-

2.4. Feeding activity by C. neritea in the presence of damaged conspeciﬁcs ment (larger number of individuals in trampled plots) (F(1,24) = 6.58; p b 0.01) and food treatment (more individuals in plots with food)

The next experiment was aimed at testing the hypothesis that dam- (F(1,24) = 95.57; p b 0.0001) (Table 2). Significant differences were aged C. neritea specimens either act as food or as a danger signal to the also found over time (F4.5,24 =11.27;pb 0.0001). The number of snails other snails approaching the food. A total of 36 plots of 1 m2 were that emerged on the surface increased in all cases when the tide rose marked out: clam carrion was placed in 9 plots, recently deceased and water reached the plots (Fig. 3), but interactions were not found C. neritea specimens were placed in another 9 plots, a mixture of clam in this case. carrion + recently deceased snails were placed in a third group of 9 plots, and the final group of 9 plots were considered as controls and 3.3. Feeding activity by C. neritea in the presence of damaged conspecifics did not contain any clams or snails. In plots with carrion, 6 pieces of razor clam (ca. 5 g each) were randomly deposited on each plot. In The abundance of C. neritea observed on the carrion or found lying plots that only contained recently deceased C. neritea, 6 pieces of on the sand varied significantly between treatments (on the carrion: crushed snail (ca. 5 g each) were randomly deposited on each plot. In F(3,36) = 4.66 and p b 0.01; on the sand: F(3,36) = 19.29 and plots with carrion plus recently deceased snails, 6 pieces each of the p b 0.0001) and these patterns proved to be consistent over time (on above samples (ca. 5 g) were randomly deposited. Every 5 min over a the carrion: F(3.6,36) = 4.32 and p b 0.001; on the sand: F(3.6,36) =5.56 period of 35 min the number of C. neritea specimens that had arrived and p b 0.0001) (Table 3). Significant interactions were not found to feed on the carrion and those on the surface of the plots that did not make contact with the carrion, were counted. Table 1 Results from a repeated-measures ANOVA, showing differences in Cyclope neritea abun- 2.5. Statistical analyses dance with time, as a within-subject factor, and treatment (trampled vs undisturbed), as an among-subject factor. Degrees of freedom: df. ***p b 0.0001.

The differences between treatments for all experimental designs df MS F were analyzed by repeated analysis of variance, with sampling time Within-subject test (Greenhouse–Geisser correction) used as a within-subject factor and the other treatments (disturbed vs. Time 7.62 0.633 8.400*** undisturbed; food supply vs. no food supply; damaged conspeciﬁcs vs. Time × Treatment 7.6 0.335 4.452*** Error 167.5 0.075 no damaged conspeciﬁcs) as among-subject factors. As the sphericity assumption was violated (Mauchly's sphericity test), the Greenhouse– Among-subject test Geisser correction was applied. In some cases, the data was log Treatment 1 13.439 216.550*** Error 22 0.062 (x + 1) transformed prior to analysis after verifying the homogeneity 4 F.J. García-García et al. / Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6

Table 2 Results from a repeated-measures ANOVA, showing differences in Cyclope neritea abundance with time, as a within-subject factor, and treatment (trampled vs undisturbed) and the presence of food, as among-subject factors. Degrees of freedom: df. ***p b 0.0001; **p b 0.01.

df MS F

Within-subject test (Greenhouse–Geisser correction) Time 4.46 0.378 11.27*** Time × Treatment 4.46 0.014 0.40 Time × Food 4.46 0.058 1.73 Time × Treat. × Food 4.46 0.031 0.91 Error 89.27 0.034

Among-subject test Treatment 1 1135 6.58** Food 1 16,480 95.57*** Treatment × Food 1 0.317 1.84 Fig. 2. Mean (±S.E.; n = 12) abundance of C. neritea specimens for each period of 15 min Error 20 0.172 after the start of the experiment. Circles, trampled plots; triangles, undisturbed plots; dashed line, distance from the plots to the tidal line.

shellfishermen are discarding bivalve carrion along the beach. It seems between treatments and time for the abundance of specimens on carri- that trophic facilitation exists between C. neritea and shellfishermen be- on, but significant interactions were found when considering the spec- cause C. neritea came to the surface in the trampled plots even in the ab- imens lying on the sandy ground (F(11.8,36) = 2.14 and p b 0.01). The sence of food on the ground. Furthermore, trampling appears to abundance of snails on the carrion was significantly higher in plots increase the snails' activity, which enables them to find food more that contained only clam carrion when compared to other treatments easily. (SNK tests; p b 0.05; Fig. 4a). However, the abundance did not differ sig- The presence of carrion in the intertidal zone is an ephemeral re- nificantly between plots treated with clam carrion + damaged snails source that is affected by the rhythm of the tides (Morton and Jones, and those with damaged snails or between the latter and the control 2003), which in turn also influences the scavenger populations. There- plots (SNK tests, p N 0.05). On the other hand, the abundance of fore, the presence of discarded animal carcasses increases the abun- C. neritea that did not make contact with the food was similar in clam dance of scavengers (Schlacher et al., 2013). For example, carrion may carrion and clam carrion + damaged snail treatments and was signifi- result from the activities of benthic predators (Oliver et al., 1985) and cantly higher than that found for the other treatments (SNK tests; waders (Daleo et al., 2005). As it occurs on the Levante beach, p b 0.05; Fig. 4b). shellfishing on sandy beaches provides a source of dead and dying bivalves that are consumed by scavengers. In addition, during the extrac- 4. Discussion tion of bivalves, shellfishermen continuously move along the tide line while it is ebbing. Our data on the effect of food and the action of tram- C. neritea responds to the presence of food by rising to the surface. pling on the activity of C. neritea demonstrate that the presence of carri- However, in the absence of carrion, the specimens remain buried on stimulates the emersion of the snail during low tide and this process throughout the tidal cycle until the plots are flooded during the rising is reinforced when trampling occurs. tide. For the first time, the results obtained in this work show, how Invertebrate scavengers have a trade-off between rising to the sur- the mechanical effect of human trampling on sandy beaches may influ- face to obtain food or staying buried to evade predators (Daleo et al., ence the behavior of C. neritea, which emerges from the sand despite the 2012). In some cases, the vibration transmitted through the sediment absence of food. It is not known whether mechanical disturbance due to by waders leads to the emersion of invertebrates, thus facilitating pre- trampling by shellfishermen serves as a warning to scavengers with re- dation by birds (Cestari, 2009; Keeley, 2001; Pienkowski, 1983). In the spect to the possible presence of fresh carrion. Nevertheless, the results case described here, the mechanical perturbation through the sediment of the present study imply that scavenger snails, such as C. neritea,are is considered to be a negative factor for invertebrates that inhabit the in- sensitive to human trampling over the sediment in which they are bur- tertidal environment. Wading birds are potential predators of C. neritea ied and this induces their rise to the surface during a time in which in the area under investigation. However, C. neritea remains were not detected in the feces or pellets of these birds on Levante beach (Pérez- Hurtado, personal observation), a finding that supports the view that there are no major risks of predation at low tide for this gastropod. Therefore, the emergence of the gastropods from the sediment, even

Table 3 Results from a repeated-measures ANOVA, showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time, as a within-subject factor, and treatment (control, food supply, food supply + injured conspeciﬁc, injured conspeciﬁc), as an among-subject factor. Degrees of freedom: df. ***p b 0.0001; **p b 0.001; *p b 0.01.

df MS F df MS F

On carrion On sand

Within-subject test (Greenhouse–Geisser correction) Time 3.60 0.086 4.32** 3.93 0.157 5.56*** Time × Treatment 10.80 0.031 1.57 11.79 0.060 2.14* Error 115.25 0.020 125.77 0.028 Fig. 3. Mean (±S.E.; n = 6) abundance of C. neritea specimens during the experiment. Among-subject test Black circle, trampled plots with clam carrion; white circle, trampled plots without clam Treatment 3 0.930 4.66** 3 3523 19.29*** carrion; black triangle, undisturbed plots with clam carrion; white triangle, undisturbed Error 32 0.200 32 0.183 plots without clam carrion; dashed line, distance from the plots to the tidal level. F.J. García-García et al. / Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6 5

In the study area C. neritea were normally observed feeding on razor clams, S. marginatus, crushed and discarded by shellfishermen and also on the fleshy remains of Cerastoderma edule and Mactra spp., which had previously been opened and partially consumed by Oystercatchers (Haematopus ostralegus). The scavenging snail also feeds on the corpses of fish and marine invertebrates such as shrimps and crabs. However, there is no evidence of cannibalism in the specimens of C. neritea (García and Pérez-Hurtado, personal observation). This situation is consistent with C. neritea declining to approach the remains of conspecifics. Based on the information described above, it can be concluded that mechanical disturbance caused in sediment due to trampling by shellfish gatherers could induce C. neritea to emerge from the sand, even when the natural tendency is to remain buried as no food is available. The presence of carrion on the ground also influences the activity of C. neritea at low tide, with an increase in its activity in areas additionally disturbed by trampling. Furthermore, despite the tendency of C. neritea to emerge when clam carrion is available persists in the presence of damaged conspecifics, the number of specimens that make contact with food is nevertheless low. This finding could indicate that the de- fense mechanism through which olfactory signals are transmitted between conspecifics is limited to distances of a few centimeters during the ebbing tide. This stimulus would therefore not be an effective and preventive signal against predators.

Fig. 4. a) Mean (±S.E.; n = 9) abundance of C. neritea specimens on clam carrion or damaged gastropods during the experiment. b) Mean (±S.E.; n = 9) abundance of C. neritea Acknowledgments specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment. Diamonds, plots with clam carrions; black squares, plots with clam We thank the authorities of the “Los Toruños” Metropolitan Park and carrions and injured gastropods; inverted triangles, plots with injured gastropods; dark circle, control plots. Cadiz Bay Natural Park (Cadiz) for permission to carry out this study and its staff for facilities provided for access to the beaches during sampling. M.C. Ruiz-Delgado was supported by the Spanish Ministry of Education when there is no food on the surface, suggests that the effect of tram- through a predoctoral grant (FPU) (AP-2009-3906). This work was sup- pling by shellfishermen harvesting S. marginatus in the sediment could ported by the incentive program to support excellent research projects, serve as a positive stimulus for C. neritea facilitating food detection, rath- financed by the Government of Andalucía (Spain) (P09-HUM-4717). er than a negative stimulus that increases the likelihood of predation. [ST] The variation in the behavior of C. neritea observed in undisturbed plots over the tidal cycle, i.e. emergence when the sand is covered References with water during high tide, indicates a relationship between the tide pattern and the activity of this snail regardless of stimuli such as tram- Andersen, A.N., 1995. Resistance of Danish coastal vegetation types to human trampling. Biol. Conserv. 71, 223–230. pling or food. Similar behavior for the gastropod Polynice incei was de- Ansell, A.D., 2001. Dynamics of aggregations of a gastropod predator/scavenger on a New scribed by Kitching et al. (1987), who correlated the activity patterns Zealand harbour beach. J. Molluscan Stud. 67, 329–341. of this species with the tides and noted activity peaks approximately Bachelet, G., Simon-Bouhet, B., Desclaux, C., García-Meunier, P., Mairesse, G., de one hour after the tidal peaks. However, this behavior is not general Montaudouin, X., Raigné, H., Randriambao, K., Sauriau, P.G., Viard, F., 2004. Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea: origin and ef- for all gastropod species; for example, the nassariid Nassarius dorsatus fects on resident fauna. Mar. Ecol. Prog. Ser. 276, 147–159. retreats into the sand when contact is made by the rising tide (Morton Barton, P.S., Cunningham, S.A., Lindenmayer, D.B., Manning, A.D., 2013. The role of carrion and Jones, 2003). in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171 (4), 761–772. 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