Marine Ecology. ISSN 0173-9565 ORIGINAL ARTICLE Loggerhead sea turtles (Caretta caretta) as bioturbators in neritic habitats: an insight through the analysis of benthic molluscs in the diet Bojan Lazar1,2,3, Romana Gracˇan4, Jelena Katic´5, Dusˇan Zavodnik6, Andrej Jaklin6 & Nikola Tvrtkovic´1 1 Department of Zoology, Croatian Natural History Museum, Zagreb, Croatia 2 Blue World Institute of Marine Research and Conservation, Veli Losˇinj, Croatia 3 Present address: Department of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia 4 Department of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia 5 Institute for Medical Research and Occupational Health, Zagreb, Croatia 6 Center for Marine Research, Ruder Bosˇkovic´ Institute, Rovinj, Croatia Keywords Abstract Adriatic Sea; bioturbation; ecological role; feeding ecology; Mollusca; sea turtles. Molluscs are a diverse and ubiquitous group of organisms which contribute to the formation of biogenic sediments and are one of the major prey taxa for the Correspondence neritic-stage loggerhead sea turtles (Caretta caretta) worldwide. Here we inves- Bojan Lazar, Department of Biology, Faculty tigated to what degree molluscs contribute to the diet of individual turtles, and of Science, University of Zagreb, 6 Roosevelt what role the feeding strategy of loggerheads might play in bioturbation, one Sq., HR-10000 Zagreb, Croatia. of the key processes in nutrient transport in marine ecosystems. We performed E-mail: [email protected] a detailed analysis of benthic molluscs from the digestive tracts of 62 logger- Accepted: 28 July 2010 head sea turtles (curved carapace length: 25.0–85.4 cm) found in the Northern Adriatic Sea. From 50 of the turtles that contained benthic molluscs, we identi- doi:10.1111/j.1439-0485.2010.00402.x fied 87 species representing 40 families and three classes (Gastropoda, Bivalvia and Scaphopoda), including 72 new dietary records for loggerhead turtle. Most of the identified molluscs were small-sized species (shell length £ 3 cm) and were often found in a subfossil condition. Their intake may be considered a byproduct of infaunal mining, while larger molluscs were mainly found crushed into smaller fragments. Through such foraging behaviour loggerheads actively rework sediments, increase the surface area of shells and the rate of shells disintegration, acting as bioturbators in this system. We conservatively estimate that loggerheads in the neritic zone of the Adriatic Sea bioturbate about 33 tonnes of mollusc shells per year, and hypothesize about the possible effects of bioturbation reduction on environmental changes in the Northern Adriatic ecosystem. & Jackson 2003). Knowledge on the role of sea turtles in Problem the ecosystems they utilize is necessary for our ability to The issue of the present and past roles of sea turtles in eco- predict how natural and anthropogenic-driven environ- systems is underlined as one of the global research priori- mental changes can affect their populations in order to ties for sea turtle management and conservation in the 21st make informed management decisions (Bjorndal 2003). century (Hamann et al. 2010). Sea turtles act at multiple Loggerhead sea turtle, Caretta caretta (Linnaeus, 1758) levels, as predators, prey, competitors, substrate for epi- is an endangered (IUCN 2009), large, long-lived top bionts, hosts of parasites and pathogens, nutrient trans- predator in marine ecosystems, with a complex life his- porters and modifiers of habitats (Bjorndal 2003; Bjorndal tory characterised by switching between different habitats Marine Ecology 32 (2011) 65–74 ª 2010 Blackwell Verlag GmbH 65 Loggerhead turtles as bioturbators Lazar, Gracˇan, Katic´, Zavodnik, Jaklin & Tvrtkovic´ (Bolten 2003; Casale et al. 2008a) and shifts in trophic status and ecological roles (Bjorndal 2003). Although the species is carnivorous generalist, exhibiting differences in the diet composition between populations and regions (Bjorndal 1997), molluscs represent one of the major prey groups for the neritic-stage loggerheads worldwide (Dodd 1988; Laurent & Lescure 1994; Limpus & Limpus 2003; Lazar et al. 2006; Casale et al. 2008a). Molluscs are diverse and ubiquitous organisms with important roles in ecosystems, such as biodeposition, pre- dation, boring, grazing, suspension and deposit feeding. Nearly all molluscs produce shells which mainly consist of calcium carbonate (Gutie´rrez et al. 2003). The shell remains stable on the sea floor after the animal dies, form- ing biogenic sediments together with the skeletal remains of other marine species (Kidwell 1985; de Bruyne 2004). Biological reworking of sediments by different organisms, Fig. 1. Study area of the Northern Adriatic Sea (northward from the from microbes and rooting plants to burrowing animals, dashed line), with bathymetry and direction of major sea currents. is termed bioturbation (Meysman et al. 2006). These organisms–sediment interactions, which structure the sub- surface of both terrestrial and marine ecosystems and play shelf (<200 m in depth) covering about 74% of the sur- a major role in biogeochemical processes, are considered face area (Fig. 1). Its northern part is <100 m in depth to be at least as important as the trophic interactions clas- and under permanent influx of fresh water, mainly arriv- sically studied by ecologists (Reise 2002). Modification of ing from the Po River (Cushman-Roisin et al. 2001). We the sediment texture, bio-irrigation and dispersal of solid carried out the present study in the Northern Adriatic particles are major biogeochemical implications of biotur- Sea, which hosts one of the largest neritic foraging habi- bation, which affect transport of nutrients in the marine tats for loggerhead turtles in the Mediterranean (Lazar & ecosystems and formation of seascapes; however, the Tvrtkovic´ 2003; Margaritoulis et al. 2003; Lazar et al. actual mechanisms behind bioturbation are less estab- 2004). The Northern Adriatic bottom consists of three lished (Meysman et al. 2006). sediment types: sand (mean grain size: 360 lm), mud The present study focuses on the bioturbating role of (mean grain size: 70 lm) and areas with a mixture of loggerhead turtles in the neritic foraging habitats of the these two sediment types (Vatova 1949; Fedra et al. Northern Adriatic Sea based upon detailed qualitative and 1976). The majority of carbonates in the sediments are of quantitative analysis of benthic molluscs in the diet of biogenic origin (Vdovic´ & Juracˇic´ 1993). this sea turtle species. We selected benthic molluscs for So far, no complete list of marine mollusc species exists two specific reasons. First, the majority of carbonates in for the Adriatic Sea. However, several studies which par- Adriatic sediments originate from shell and skeletal frag- tially described the distribution of benthic marine flora ments (Vdovic´ & Juracˇic´ 1993). Secondly, a recent study and fauna (e.g. Vatova 1935, 1949; Zavodnik 1971; on the feeding ecology of loggerhead turtles in the Adriat- Hrs-Brenko et al. 1994; Jaklin & Arko-Pijevac 1997) ic Sea emphasized molluscs as the major prey group in defined the Northern Adriatic Sea as an area with high their diet, accounting for 41.1% of dry mass (Lazar macrofaunal density, including a high diversity of molluscs 2009). The aim of this study was therefore to investigate (Vatova 1949; Gamulin-Brida 1967; Scaccini 1967; Fedra to what degree a dietary regime largely based upon mol- et al. 1976; Zavodnik & Vidakovic´ 1987; McKinney 2007). luscs, together with loggerhead feeding behaviour in neri- tic areas (Preen 1996; Houghton et al. 2000; Schofield Material and Methods et al. 2006), may contribute to the individual intake (energy gain by feeding) and what is the possible role of We performed general necropsies of 62 loggerhead sea such feeding strategy in bioturbation. turtles with notch-tip curved carapace length (CCL) rang- ing between 25.0 and 85.4 cm (mean CCL = 45.1 ± 14.3 cm), found stranded or incidentally captured dead Study Area by fisheries in the Northern Adriatic Sea (Slovenia and The Adriatic Sea is a relatively shallow (mean depth: Croatia) in 1995–2004. We isolated the oesophagus, 239 m), temperate, semiclosed sea, with the continental stomach and intestinal tracts, rinsed gut contents in clear 66 Marine Ecology 32 (2011) 65–74 ª 2010 Blackwell Verlag GmbH Lazar, Gracˇan, Katic´, Zavodnik, Jaklin & Tvrtkovic´ Loggerhead turtles as bioturbators water through a 1-mm mesh sieve, and preserved samples classes: Gastropoda (601 specimens), Bivalvia (123 speci- in 4% buffered formaldehyde. All benthic mollusc shells mens) and Scaphopoda (2 specimens). The average num- were isolated and identified under a stereomicroscope to ber of shells per individual turtle was 14.5 ± 24.1, and the the lowest taxon possible. The taxonomic nomenclature maximum number of molluscs was 132, isolated from a used follows the European Register of Marine Species turtle of 70.0 cm CCL. (ERMS, Costello et al. 2008). We counted ingested speci- We have identified 91 taxa of benthic molluscs, including mens when possible, either based upon the number of 87 species representing 40 families, and recorded 72 new whole shells or upon the number of apertures (in the case species in the diet of loggerhead turtles: 37 gastropods, 34 of crushed shells of gastropods) and calculated the per- bivalves and one scaphopod. Most of the identified spe- cent of occurrence for each species. cies belonged to gastropods (50 species, 57.5%), followed To differentiate