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Apparent Resource Partitioning and Trophic Structure of Large-Bodied Marine Predators in a Relatively Pristine Seagrass Ecosystem

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Apparent Resource Partitioning and Trophic Structure of Large-Bodied Marine Predators in a Relatively Pristine Seagrass Ecosystem Vol. 481: 225–237, 2013 MARINE ECOLOGY PROGRESS SERIES Published May 7 doi: 10.3354/meps10235 Mar Ecol Prog Ser Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem Michael R. Heithaus1,*,**, Jeremy J. Vaudo1,**, Sina Kreicker2, Craig A. Layman1, Michael Krützen2, Derek A. Burkholder1, Kirk Gastrich1, Cindy Bessey1, Robin Sarabia1, Kathryn Cameron1, Aaron Wirsing3, Jordan A. Thomson1, Meagan M. Dunphy-Daly4 1Marine Sciences Program, School of Environment, Arts and Society, Florida International University, 3000 NE 151st St., North Miami, Florida 33181, USA 2Evolutionary Genetics Group, Anthropological Institute & Museum, University of Zurich, Winterthurerstr. 190, 8057 Zurich, Switzerland 3School of Environmental and Forest Sciences, Box 352100, University of Washington, Seattle, Washington 98195, USA 4Duke University Marine Laboratory, Nicholas School of the Environment, 135 Duke Marine Lab Road, Beaufort, North Carolina 28516, USA ABSTRACT: Large predators often play important roles in structuring marine communities. To understand the role that these predators play in ecosystems, it is crucial to have knowledge of their interactions and the degree to which their trophic roles are complementary or redundant among species. We used stable isotope analysis to examine the isotopic niche overlap of dolphins Tursiops cf. aduncus, large sharks (>1.5 m total length), and smaller elasmobranchs (sharks and batoids) in the relatively pristine seagrass community of Shark Bay, Australia. Dolphins and large sharks differed in their mean isotopic values for δ13C and δ15N, and each group occupied a rela- tively unique area in isotopic niche space. The standard ellipse areas (SEAc; based on bivariate standard deviations) of dolphins, large sharks, small sharks, and rays did not overlap. Tiger sharks Galeocerdo cuvier had the highest δ15N values, although the mean δ13C and δ15N values of pigeye sharks Carcharhinus amboinensis were similar. Other large sharks (e.g. sicklefin lemon sharks Negaprion acutidens and sandbar sharks Carcharhinus plumbeus) and dolphins appeared to feed at slightly lower trophic levels than tiger sharks. In this seagrass-dominated ecosystem, seagrass- derived carbon appears to be more important for elasmobranchs than it is for dolphins. Habitat use patterns did not correlate well with the sources of productivity supporting diets, suggesting that habitat use patterns may not necessarily be reflective of the resource pools supporting a popula- tion and highlights the importance of detailed datasets on trophic interactions for elucidating the ecological roles of predators. KEY WORDS: Food webs · Predator–prey interactions · Stable isotope · Niche overlap · Elasmobranchs · Sharks · Cetacean · Trophic redundancy · Niche partitioning Resale or republication not permitted without written consent of the publisher INTRODUCTION both consumptive and non-consumptive effects on their prey (e.g. Williams et al. 2004, Heit haus et al. Large-bodied marine predators, especially sharks 2008, 2010, Wirsing et al. 2008). In many cases, how- and odontocete cetaceans (toothed whales), can play ever, our understanding of the ecological role of important roles in coastal marine communities through these taxa is hindered by a lack of information on *Email: [email protected] © Inter-Research 2013 · www.int-res.com **These authors contributed equally to this work 226 Mar Ecol Prog Ser 481: 225–237, 2013 their trophic interactions and the degree of re source we investigated (1) trophic positions and isotopic partitioning or trophic redundancy that may exist niches (see Newsome et al. 2007) of the common within this guild of large marine predators (e.g. large-bodied (>1.5 m) predators, (2) overlap of iso- Kitchell et al. 2002, Heithaus et al. 2008, Ferretti et al. topic niches among species and higher-order taxa 2010). Often, this lack of information can be attrib- (i.e. the potential for resource partitioning), (3) the uted to the difficulty in obtaining adequate sample relationships between body size and relative trophic sizes for stomach content analysis. Yet, understand- position, and (4) the possibility for individual level ing the trophic interactions and positions of large- dietary specialization in trophic interactions within bodied predators is an important step in elucidating populations of common species. the dynamics of marine communities (e.g. Williams et al. 2004, Lucifora et al. 2009) and the potential for top predators to couple various trophic pathways (e.g. MATERIALS AND METHODS Rooney et al. 2006). In many systems, there is a high degree of interspe- Study site cific differentiation in the diets and trophic inter - actions of sympatric species of large-bodied sharks Shark Bay is a ca. 13000 km2 subtropical embay- and odontocetes. For example, in the southwest ment along the central coast of Western Australia. Indian Ocean, sympatric species of small odontocetes The bay contains ca. 4000 km2 of seagrass beds and is forage at different trophic levels or from different perhaps one of the most pristine seagrass ecosystems food web modules (Kiszka et al. 2011). Off the coast left in the world (e.g. Heithaus et al. 2008). In addition of South Africa, most species of dolphins and sharks to seagrasses, the primary sources of productivity that show relatively low dietary overlap (Heithaus 2001a). support food webs in Shark Bay in clude plankton and Resource partitioning, however, is not ubiquitous, macroalgae (e.g. Burkholder et al. 2011, Heithaus et and substantial dietary overlap has been documen - al. 2011). The bay contains substantial populations of ted among sympatric large shark species as well as large vertebrates, including herbivorous green turtles between shark and dolphin populations. For exam- Chelonia mydas and du gongs Dugong dugon and ple, off the coast of South Africa, there is significant predators such as loggerhead turtles Caretta caretta, dietary overlap between several species of large Indo-Pacific bottlenose dolphins Tursiops cf. aduncus, sharks and common dolphins Delphinus delphis and a variety of sharks. The shark fauna is dominated (Heithaus 2001a). Also, off the Pacific coast of Costa numerically by tiger sharks Galeocerdo cuvier (Hei- Rica, silky sharks Carcharhinus falciformis and com- thaus 2001b, Wirsing et al. 2006), which account for mon bottlenose dolphins Tursiops truncatus compete >90% of captures of sharks over 1.5 m total length for fish prey (Acevedo-Gutiérrez 2002). Gaining fur- (Heithaus et al. 2012). Tiger sharks in Australia con- ther insights into potential overlap or divergence in sume a wide range of prey, including teleosts, trophic interactions of upper trophic level predators cephalopods, sea snakes, sea turtles, marine birds, is important because the degree of trophic redun- and marine mammals (Simpfendorfer 1992, Heithaus dancy and intraguild predation (when predator and 2001a, Simpfen dorfer et al. 2001). The proportion of prey also compete for resources) play important roles large-bodied prey in tiger shark diets increases with in community stability (e.g. Bascompte et al. 2005, shark size (Simpfendorfer 1992, Simpfendorfer et al. Kondoh 2008). 2001). Other species of large sharks in Shark Bay are In the absence of extensive stomach content data, primarily from the genus Carcharhinus. In locations stable isotopes can provide important insights into where their diets have been studied, these species variation in trophic interactions both within and feed primarily on teleosts and cephalopods (Cortés among species (e.g. Bearhop et al. 2006, Quevedo et 1999). The pigeye shark Carcharhinus amboinensis, al. 2009, Layman et al. 2012), albeit over different however, tends to include a high proportion of temporal scales and with different resolution than elasmo branchs in its diet (Cortés 1999), as does the information derived from stomachs. We used stable occasionally encountered great hammerhead shark isotopes to investigate the trophic relationships of Sphyrna mokarran (Stevens & Lyle 1989, Cortés large-bodied sharks and a resident odontocete ceta - 1999). Smaller sharks and dolphins in the study area cean within a relatively pristine coastal seagrass are largely piscivorous (e.g. Cortés 1999, Heithaus & ecosystem — Shark Bay, Australia — that has been Dill 2002, White et al. 2004). used as a model system for understanding the eco- Since 1997, we have used the Eastern Gulf of Shark logical role of large marine vertebrates. Specifically, Bay, along the eastern coast of Peron Peninsula, as a Heithaus et al.: Isotopic niches of predators in a seagrass ecosystem 227 model system for understanding the behavior and in a saturated NaCl and 20% dimethyl-sulfoxide ecological role of large marine vertebrates, particu- (DMSO) solution (Amos & Hoelzel 1992) at −20°C in larly tiger sharks and large grazers (see Heithaus et the field and −80°C in the laboratory. Prior to stable al. 2008, 2009). This area has also been the site of isotope analysis, the epidermal skin was removed long-term research on the behavior and ecology of from each sample. Lipid extraction of cetacean skin Indo-Pacific bottlenose dolphins (Connor & Smolker samples stored in DMSO is a commonly used method 1985, Smolker et al. 1992). Large sharks tend to be for removing the effect of DMSO preservation on iso- seasonally abundant in the study area, with high topic signatures (Todd et al. 1997, Marcoux et al. densities found in the warm months (September
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