Journal of Experimental Marine Biology and Ecology 467 (2015) 1–6 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe 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 preda- tion 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 ma- rine 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 spe- cies 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.