Vol. 439: 263–276, 2011 MARINE ECOLOGY PROGRESS SERIES Published October 20 doi: 10.3354/meps09327 Mar Ecol Prog Ser Communal or competitive? Stable isotope analysis provides evidence of resource partitioning within a communal shark nursery Michael J. Kinney1,*, Nigel E. Hussey2, Aaron T. Fisk2, Andrew J. Tobin1, Colin A. Simpfendorfer1 1Fishing and Fisheries Research Centre, School of Earth and Environmental Sciences, James Cook University, Townsville, Queensland 4811, Australia 2Great Lakes Institute for Environmental Science, University of Windsor, 401 Sunset Avenue, Windsor, Ontario N9B 3P4, Canada ABSTRACT: Quantifying the diet of sympatric co-occurring predatory species is a challenging task, made more so when investigations attempt to focus on specific age groups. This is the task that confronts efforts to understand dietary resource partitioning among co-occurring juvenile shark species within nursery areas. Here, stable isotope analysis (δ13C and δ15N) is used to over- come these challenges in describing species dietary resource partitioning strategies within the communal shark nursery area of Cleveland Bay, Queensland, Australia. We analyzed the isotopic composition of 3 distinct tissues, (muscle, blood plasma, and red blood cells), for 7 species of shark and 3 species of large predatory teleost to investigate whether these communal areas support their diverse array of predators without the need for resource partitioning strategies. Clustered δ15N values for all examined species indicated feeding within the same trophic level; however, wide ranging δ13C values denoted exploitation of several primary carbon sources. Our results demon- strate inter-species resource partitioning strategies at work within the examined communal shark nursery, altering the previous interpretation of these areas as resource-rich and/or competition- limited environments. KEY WORDS: Coastal · Dietary overlap · Muscle · Niche partitioning · Plasma · Red blood cells Resale or republication not permitted without written consent of the publisher INTRODUCTION few years of life with little to no competition (Bran - stetter 1990, Salini et al. 1992, Castro 1993, Simpfen - The use of discrete inshore shallow water areas as dorfer & Milward 1993). nurseries by juvenile sharks has been established in More recent shark nursery area studies are finding the scientific literature since the mid twentieth cen- evidence countering the theory of nursery area tury (Springer 1967). Over time many aspects of the resource abundance. Evidence of slow growth rates original shark nursery area theory have been altered, (Bush & Holland 2002, Lowe 2002, Duncan & Holland omitted, or added to, but the central paradigm has 2006) and high mortality rates of young sharks in persisted. One of the longest standing tenets of the nursery areas has been attributed in part to a lack of nursery area paradigm is the theory of resource sufficient food resources (Manire & Gruber 1993, abundance — the idea that young sharks can remain Duncan & Holland 2006). In the Gulf of Mexico, mor- in the nursery while feeding and growing for the first tality rates of up to 90% for juvenile blacktip sharks *Email: [email protected] © Inter-Research 2011 · www.int-res.com 264 Mar Ecol Prog Ser 439: 263–276, 2011 Carcharhinus limbatus within Terra Ceia Bay, Flo - a rate of approximately 2 to 4‰ of δ15N with each rida, USA, were attributed to natural mortality, inclu - step up in trophic level (Peterson & Fry 1987, Mich- ding predation, starvation, and disease (Heupel & ener & Schell 1994, Post 2002), making it possible to Simpfendorfer 2002). These findings provide strong model an organism’s relative trophic position within evidence that the view of nursery areas as protective, a given ecosystem. resource abundant reserves for young sharks is out- Stable isotope analysis (SIA) provides many bene- dated and no longer fits much of the current data fits over traditional stomach content analysis: (1) it (Heupel et al. 2007). represents assimilated, not just ingested, prey items While evidence of resource limitations within sin- (Bearhop et al. 2004, Domi et al. 2005); (2) isotopic gle species nursery areas is mounting, few studies values represent long-term feeding behaviours (from have investigated resource partitioning among co- months to years depending on the tissue analyzed) occurring shark species (Salini et al. 1992, Platell et (Domi et al. 2005, MacNeil et al. 2005, 2006); (3) sam- al. 1998, Bethea et al. 2004, White et al. 2004), with pling multiple tissues can provide distinct timeframes only Bethea et al. (2004) focusing specifically on due to differences in tissue turnover rates (Kurle & juveniles in these areas. Although these studies have Worthy 2002, MacNeil et al. 2005); and (4) samples found some evidence of resource partitioning, sev- from several different tissues can be obtained with- eral limitations inherent to stomach content analysis out the need to euthanize animals. SIA therefore pro- have made determining broad-scale resource parti- vides a useful tool to investigate questions such as tioning difficult. These include: the snapshot nature dietary resource partitioning within communal shark of stomach content data (Pinnegar & Polunin 1999, nursery areas. Pinnegar et al. 2001, Bearhop et al. 2004, MacNeil et While a number of SIA studies have been carried al. 2005), the persistence of hard structures like out on the structure of marine food webs (Hobson & cephalopod beaks and crustacean shells (Wilson et Welch 1992, Michener & Schell 1994, Hobson et al. al. 1985) and, in the case of animals such as sharks, 2002), and focusing on specific teleost species the preponderance of empty stomachs and unidenti- (Thomas & Cahoon 1993, Das et al. 2000, Harvey et fiable prey items (Cortés 1997). These limitations al. 2002, Cunjak et al. 2005, Perga & Gerdeaux 2005, typically necessitate large sample sizes (Cortés 1997, Schlacher et al. 2005), little research has been pub- 1999, Estrada et al. 2005, MacNeil et al. 2005), which lished on SIA for sharks. These include a handful of however are often feasible either due to simple pro- field studies that focus on sharks and rays (Fisk et al. ject logistics or concerns over a species’ conservation 2002, Estrada et al. 2003, Domi et al. 2005, MacNeil status (Heupel & Simpfendorfer 2010). These prob- et al. 2005, Estrada et al. 2006, Kerr et al. 2006, lems are compounded further when an investigation McMeans et al. 2009), and only 3 laboratory studies: seeks to understand the diet of a select size or age MacNeil et al. (2006), who assessed variable uptake range, for example the diet of young sharks within and elimination of carbon and nitrogen isotopes in nursery areas. the tissues of freshwater ocellate river stingrays Pota- One way to address the limitations of stomach con- motrygon motoro; Hussey et al. (2010a), who looked tent analysis is through the use of naturally occurring at diet-tissue discrimination factors in large sharks stable isotopes of carbon (δ13C) and nitrogen (δ15N). held under semi-controlled conditions; and Logan & This technique has emerged as a powerful alterna- Lutcavage (2010), who investigated the effects of diet tive or complementary tool for assessing the feeding switching on captive sandbar sharks Carcharhinus ecology of organisms (Domi et al. 2005). The plumbeus. approach is based on the principle that the stable iso- The present study utilized SIA of multiple tissues tope ratios in consumer tissues can be related in a representing variable integration periods to assess predictive way to those in their diet (DeNiro & the extent of dietary resource partitioning by 7 of the Epstein 1978, 1981). Values of δ13C can be used to most commonly occurring juvenile shark species, as track sources of primary carbon, as δ13C shows rela- well as 3 large predatory teleost species, within an tively little change between trophic levels (~1‰ per established communal shark nursery area (Simpfen- trophic level) from primary producers up through dorfer & Milward 1993). The juvenile shark species apex predators (Peterson & Fry 1987, Hobson & examined were distributed throughout the nursery, Welch 1992). As such, δ13C can be a useful indicator displayed varying degrees of spatial and temporal of sources of primary productivity in simple systems overlap, and rarely left the nursery during early life where at least 2 isotopically distinct sources are pre- (M. J. Kinney unpubl. data). Therefore, comparisons sent (Hobson et al. 1995). Enrichment of 15N occurs at of stable isotope values between species were not Kinney et al.: Resource partitioning in a communal shark nursery 265 compromized by spatial or temporal factors specific to any one section of the bay. Results from this study will further our understanding of the important eco- logical interactions at work within communal nursery areas and may assist in the prioritization of conserva- tion and management strategies for co-occurring shark species in nursery environments. MATERIALS AND METHODS Study site alues are confounded by maternal Cleveland Bay, QLD, Australia. Target Cleveland Bay, Cleveland Bay is situated east Townsville on the north-east coast of Queensland, Australia, and covers an area of approximately 225 km² from 19° 10’ to 19° 19’ S and from 146° 50’ to 147° 01’ E. The bay is shallow throughout, reaching a maximum depth of 15 m near its outer edge. The benthic environment of the bay is predominantly soft mud with some smaller areas of coastal reefs; for a