Bryan Stanley Charleston Institutes of Art Johnson and Wales

Many species of sharks (bracket Elasmobranchii) are ecologically important animals because of their role every bit predators in marine environments (Chapman et al. 2006), though decades of global overfishing take led to reported population declines in many shark species (Dulvy et al. 2008). The U.S. National Marine Fisheries Service plans to somewhen institute a new ecosystem-based fishery management plan to meliorate the management of U.South. shark species (SEDAR 2006). Ecosystem-based fisheries management plans differ from traditional fishery management by focusing not just on a target population merely also on diet, trophic interactions, and environment (Pikitch et al. 2004).

One shark species of particular concern to the National Marine Fisheries Service is the heavily exploited Sandbar Shark Carcharhinus plumbeus (SEDAR 2006). Sandbar Sharks, which are seasonally abundant in South Carolina (Castro 1993; Abel et al. 2007; Ulrich et al. 2007), take declined in population size in the western N Atlantic by 60–80%; but populations take begun to stabilize since 2007 due to catch restrictions (Romine et al. 2011; SEDAR 2011). Sandbar Sharks are born most the mouths of shallow estuaries in tardily May or early June and enter the estuaries every bit principal nurseries, remaining there until Oct or Nov (Castro 1993; Ulrich et al. 2007). After overwintering offshore, young juvenile Sandbar Sharks return to estuaries the following spring and utilize them as secondary nurseries. (Conrath and Musick 2008).

The traditional method for characterizing shark diet is tum content analysis, which has typically involved opening the shark'due south tummy and identifying the prey items found inside (Cortes 1999). Alternative nonlethal methods, such as gastric lavage and stomach eversion, have also been utilized (Shurdak and Gruber 1989). Stomach content analysis provides loftier-resolution "snapshot" diet data (Hyslop 1980; Pinnegar and Polunin 1999), though at that place are many limitations to the method. For example, predatory fishes often accept a high percent of empty stomachs (Arrington et al. 2002), which can result in having to lethally sample a larger number of specimens in society to accumulate plenty prey items to characterize a species' diet. Additionally, sharks may regurgitate due to capture stress, which increases the number of animals with empty stomachs (Stevens 1973).

An alternative method to study elasmobranch nutrition is stable isotope analysis (Hussey et al. 2011; Hussey et al. 2012; Shiffman et al. 2012). This method utilizes the isotopic signatures of carbon and nitrogen isotopes in tissues to examine trophic status and other relevant ecological relationships, such as sources of carbon to the food web (Peterson and Fry 1987). This technique can provide long-term, temporally integrated diet estimates compared with breadbasket content analysis, which reflects but recently ingested prey (Pinnegar and Polunin 1999). Gathering samples for stable isotope analysis can also be nonlethal and minimally invasive when restricted to the use of certain tissues (Sanderson et al. 2009).

This written report examines the ratios of carbon (^xiiiC/¹²C) and nitrogen (^fifteenN/¹⁴Due north) stable isotopes in muscle tissue of Sandbar Sharks in South Carolina's estuaries. Carbon isotopic ratio levels are commonly slightly enriched relative to a food source, approximately 0–1‰ relative to a standard with each trophic level increase, while nitrogen isotopic ratios typically enrich approximately three.4‰ per trophic level (Minagawa and Wada 1984; Peterson and Fry 1987). Carbon isotopic ratios are therefore useful to differentiate betwixt food spider web carbon sources (i.e., benthic versus pelagic, coastal versus offshore) and signal diet, while nitrogen isotopic ratios can signal different trophic levels (Peterson and Fry 1987; Post 2002).

While the values of three.4‰ and 0–1‰ are typical nutrition–tissue discrimination factors, these values can vary significantly by study species and tissue. A review of diet–tissue discrimination factors (Caut et al. 2009) constitute that the mean discrimination factor for nonelasmobranch fish musculus is approximately 2.5‰ for nitrogen isotopes and i.8‰ for carbon isotopes. Recent enquiry on elasmobranchs has shown that the diet–tissue discrimination factor values tin can be slightly different for these fishes, ranging from two.4‰ for nitrogen isotopes and 0.ix‰ for carbon isotopes in the muscle of the Sand Tiger Carcharias taurus (Hussey et al. 2010) to 3.7‰ for nitrogen isotopes and 1.vii ‰ for carbon isotopes in the musculus of the Leopard Shark Triakis semifasciata (Kim et al. 2012).

Though Sandbar Shark diet has never been characterized in South Carolina, stomach content analyses have been conducted on Sandbar Sharks from the coastal waters of the Hawaiian Islands (McElroy et al. 2006) and the estuarine and coastal waters of Virginia (Medved et al. 1985; Ellis and Musick 2007). These past studies noted an ontogenetic shift in diet in both regions, with immature-of-year (historic period-0) Sandbar Sharks preying primarily on benthic crustaceans, including blueish crab Callinectes sapidus and mantis shrimp Squilla empusa, and older, larger juveniles relying increasingly on modest elasmobranchs and teleost fishes. Yet, Sandbar Sharks accept many allopatric subpopulations (Compagno et al. 2005) and information technology is unknown if this diet shift occurs throughout their entire range. Other shark species, such equally the Shortfin Mako Isurus oxyrinchus (Stevens 1984; Cliff et al. 1990; Maia et al. 2006) and the Spiny Dogfish Squalus acanthias (Ellis et al. 1996; Smith and Link 2010), are known to swallow radically different types of prey in various parts of their range.

Determining whether ontogenetic diet shifts occur is important to consider when attempting to create effective ecosystem-based fisheries management plans (Lucifora et al. 2009; Simpfendorfer et al. 2011). Stable isotope analysis comparison δ¹³C and δ¹⁵Northward tissue signatures of individuals of different age-classes inside the same species has been used to find ontogenetic nutrition shifts in animals such as the dark-green bounding main turtle Chelonia mydas (Arthur et al. 2008) and Ruddy Snapper Lutjanus campechanus (Wells et al. 2008), though rarely in wild populations of sharks. Though detecting an ontogenetic shift in nutrition was not the focus of their studies, Matich et al. (2010) noted a deviation in inter-tissue isotopic signature variability betwixt smaller and larger Bull Sharks Carcharhinus leucas and Vaudo and Heithaus (2011) noted differences in boilerplate isotopic signatures between different size-classes of three species of littoral elasmobranchs. Ontogenetic nutrition shifts in sharks have been detected using other analyses of isotopic data that involved either sacrificing sharks to obtain liver samples or opportunistically utilizing vertebrae samples from sharks sacrificed for other studies (MacNeil et al. 2005; Estrada et al. 2006; Hussey et al. 2011; Malpica-Cruz et al. 2013).

Since many shark species are live bearing, the maternal contribution of isotopes to age-0 sharks must be considered when analyzing isotopic signatures of historic period-0 specimens (McMeans et al. 2009; Vaudo et al. 2010; Olin et al. 2011). Maternal investment results in higher δ¹⁵N and either higher or lower δ¹³C values in historic period-0 sharks relative to mothers (McMeans et al. 2009; Vaudo et al. 2010). Maternal contribution can also be detected past analyzing the change in isotopic signature of age-0 sharks over time equally they shift to a dietary-influenced isotopic signature (Shaw 2013). Additionally, while isotope turnover rates are generally slow in shark muscle (requiring up to 2 years for complete turnover), significant and ecologically relevant changes in Sandbar Shark musculus isotopic signature (∼2‰ for ^xiiiC and ∼5‰ for ¹⁵N) are detectable within two months of a diet switch (Logan and Lutcavage 2010). Isotopic turnover rates must also be considered when analyzing isotopic ratios from species that undergo seasonal migrations, such as Sandbar Sharks that migrate between estuarine and offshore waters (Castro 1993; Abel et al. 2007).

The goals of this study were to employ δ¹³C and δ¹⁵N stable isotope signatures of muscle tissue to characterize the diets and trophic levels of Sandbar Sharks in South Carolina estuaries and coastal waters and to determine if there are any ontogenetic, sex-based, or geographic differences in diet and trophic level. The South Carolina estuarine systems sampled differ geographically and ecologically from the more northern habitats of Virginia (Matriarch et al. 2000) and the reef-dominated habitats of Hawaii, where previous breadbasket content analyses of this species accept been conducted. Isotopic data from sympatric potential prey species in Due south Carolina were also analyzed.

METHODS

Sample collection.—Sandbar Shark muscle samples were obtained opportunistically from three coastal shark surveys. Sandbar Sharks were captured using longlines past the S Carolina Section of Natural Resources (SCDNR) Cooperative Atlantic States Shark Pupping and Nursery survey, the SCDNR Developed Scarlet Drum Sciaenops ocellatus survey, and the Coastal Carolina Academy shark survey. Five S Carolina estuaries were sampled from May through November in 2009 and 2010: Winyah Bay, Bulls Bay, Charleston Harbor, St. Helena Sound, and Port Majestic Sound (Figure 1). All Sandbar Sharks captured were sexed, measured (both fork length [FL] and stretch total length [TL]), tagged through the dorsal fin with Dalton roto-tags, and released. Dorsal muscle samples of approximately 2 g were taken from the captured Sandbar Sharks prior to release using a ii.0-mm disposable biopsy dial (Premier Medical Products Unipunch). Muscle samples were kept on ice in ii.0-mL cryovials while in the field and upon return to the laboratory were frozen at −lxxx°C until processing.

Effigy 1. Sampling sites in South Carolina estuaries and coastal waters. The dots represent longline and gillnet survey locations from the SCDNR Cooperative Atlantic States Shark Pupping and Nursery survey (COASTSPAN), while the stars represent the longline survey locations from the SCDNR Adult Blood-red Pulsate project.

Immature of year were defined every bit Sandbar Sharks less than i year old (age 0) and were identified by the presence of umbilical scarring and a FL less than 580 mm (Ulrich et al. 2007). Juveniles were older than one yr (>580 mm FL) and had no umbilical scarring but had not yet reached the reproductively mature size of approximately 1,400 mm FL (Sminkey and Musick 1996). Sandbar Sharks over 1,400 mm FL were considered adults, and since only viii developed sharks were captured during this study, adults were excluded from about analyses. Samples of co-occurring possible prey species in Due south Carolina estuarine waters, including a diversity of invertebrate and fish species, were obtained opportunistically from SCDNR inshore fisheries surveys. Whenever possible, samples of each prey species were obtained from multiple estuaries, simply individuals from unlike estuaries were grouped together for analysis.

Sample processing.—Residual peel, vanquish, or scales were removed from biopsy samples (Sandbar Sharks and co-occurring possible prey were analyzed to elucidate Sandbar Shark nutrition) using a scalpel and so that only musculus tissue was analyzed (post-obit Davenport and Bax 2002). Preliminary analysis was performed to determine whether urea removal and lipid removal were needed. This consisted of processing multiple samples from the aforementioned individual shark in four unlike ways (no lipid removal and no urea removal, urea removal and no lipid removal, lipid removal and no urea removal, and removal of both lipids and urea) and comparing results. This process was repeated for samples from x individual sharks.

To remove urea, all elasmobranch musculus tissue (Sandbar Sharks as well as rays and sharks analyzed as potential prey species) were sonicated three times in ane.0 mL of deionized water for 15 min, decanting the water in betwixt each sonication (Kim and Koch 2011). Preliminary analysis indicated that urea removal lowered δ¹⁵N signatures in elasmobranch muscle by an average of 0.5‰ and therefore urea removal was performed on all elasmobranch muscle tissue (Sandbar Sharks and co-occurring potential casualty species) analyzed in this report.

Lipid extraction is occasionally performed on muscle tissues (MacNeil et al. 2005), simply preliminary trials indicated that this method had no event on the δ¹³C signatures of shark musculus (δ^xiiiC signatures of the samples analyzed in the preliminary trials were extremely similar and considered equal between lipid extraction and nonlipid extraction processing methods). Additionally, C:N ratios were depression for Sandbar Sharks (approximately i.2), suggesting low lipid content (Post et al. 2007). Therefore lipid extraction was not utilized on elasmobranch samples in this study. Lipid extraction was, however, utilized on all musculus samples from nonelasmobranch co-occurring potential prey species. One milliliter of dichloromethane was added to each sample tube containing nonelasmobranch muscle tissue, tubes were placed in an ultrasonic water bathroom for 15 min, and the dichloromethane was and so decanted, repeating the process a total of iii times (John Kucklick, National Institutes of Science and Technology, personal communication).

All samples were then lyophilized (SP Scientific Virtis Genesis) overnight and homogenized into a fine powder using a Biospec mini dewdrop-beater eight with ane.0-mm beads. Aliquots of these powdered samples (1 mg) were measured, placed into tin capsules, and analyzed using a Thermo Flash EA coupled to a ThermoFisher Scientific Delta V Plus Isotope-ratio mass spectrometer located at the isotope laboratory at the Skidaway Plant of Oceanography (Savannah, Georgia), which has a precision of ±0.i for both carbon and nitrogen isotopes. Sample stable isotope values were calibrated against internally calibrated laboratory chitin powder standards (−0.90‰ ¹⁵N,–xviii.95‰ ¹³C), which are cross-checked against the U.S. Geological Survey twoscore international isotope standard and National Institute of Standards and Technology Standard Reference Material 8542 ANU-Sucrose.

Statistical analysis.—Stable isotope ratios were expressed in parts per thou (‰), a ratio of the isotopes in a sample relative to a reference standard. Delta notation (δ) is divers using the following equation: where X is defined equally the heavy isotope, either ^xiiiC or ¹⁵N, R _sam is the ratio of heavy to light isotopes within each sample, and R _sta is the heavy to lite ratio in a reference standard.

TABLE one. Biological and demographic data for all Sandbar Sharks sampled (total) and those from summer–fall (SF) months.

Isotopic data (δ¹³C and δ^xvN) from each muscle sample were analyzed by sampling calendar month, sampling year, sex activity, location (estuary), and age-form. Differences in δ¹³C and δ¹⁵N between sampling months, sampling years, sexes, estuaries, and age-classes were assessed by multiple-gene analysis of variance (ANOVA). First, all Sandbar Sharks were compared. Second, in order to avert maternal input bias in age-0 sharks (Olin et al. 2011) and recent offshore feeding bias in migrating juvenile sharks, but samples collected after July 15th (approximately 2 months after juvenile Sandbar Sharks typically reenter the estuary and well-nigh young of year take been born, Ulrich et al. 2007) were compared. This was considered to exist enough fourth dimension for the Sandbar Sharks' slow muscle isotopic turnover rate (Logan and Lutcavage 2010) to reflect evidence of an estuarine diet-influenced isotope signature, though likely not enough time to allow for full isotopic equilibrium to the estuarine surround. Sandbar Sharks captured after July 15 are referred to as "summer–fall" sharks hereon. Finally, to account for the unbalanced sample design, multiple ANOVAs were performed focusing on each variable to avert interaction effects (i.e., near all age-0 sharks were captured in just two estuaries, complicating analysis by estuary, and certain estuaries were sampled more in sure months, complicating analysis past month). Tests were run for both the consummate fix of all Sandbar Sharks and for summer–fall sharks only, and a Holm correction was used on the resulting P-values to reduce the take chances of type I fault. We hypothesized significant differences in both δ¹³C and δ¹⁵Due north between age-classes, which would indicate an ontogenetic nutrition shift, but did non look differences betwixt sampling years, sampling months, or sampling locations. Statistical calculations throughout the study were performed using R (R Development Core Team 2010).

Metrics for comparison of isotope ratios betwixt age-classes followed methods past Layman et al. (2007a). Metrics include δ¹⁵Northward range and δ¹³C range (the departure between the largest and smallest δ¹⁵Northward and δ¹³C values inside each age-grade), and total occupied niche area (the convex hull area of the polygon represented by all of the δ¹³C or δ¹⁵N data for each age-class). Unlike raw isotopic information, these values are suitable for comparisons between species from different habitats.

The relative trophic position of Sandbar Sharks was calculated using Post's (2002) formula. The species used to judge δ¹⁵N_base was Summer Flounder Paralichthys dentatus, a secondary consumer that was assigned a trophic level of three.0. A value of 3.7 was used for the initial value of Δ¹⁵North, the increase in the ratio of ¹⁵Due north associated with one increasing trophic level, following Kim et al. (2012). Trophic position adding requires appropriately selected nutrition–tissue discrimination factors. The primary diet–tissue discrimination factor utilized comes from Kim et al. (2012), to date the merely discrimination factors calculated for elasmobranchs using completely controlled feeding conditions. For the purpose of testing sensitivity, trophic position calculations were likewise run with nutrition–tissue bigotry factors from Hussey et al. (2010), a "semicontrolled" feeding study, and the mean values for nonelasmobranch fishes from Caut et al. (2009).

Current stable isotopic analytical techniques do not allow for the precise decision of the specific casualty species consumed by generalist predators. Though several avant-garde statistical mixing models exist, many accept very precise data requirements that were non met by this study due to the opportunistic sampling regime (samples were provided by the SCDNR inshore fisheries survey whenever possible, and samples obtained did non include principal producers). The sample size of many prey species was insufficient to infer diet with accuracy using many mixing models, and baseline data (i.due east., primary producer carbon signature) was unavailable. Multiple samples of each prey species were averaged together with the assumption that specimens from different estuaries had similar isotopic signatures.

RESULTS

A total of 262 Sandbar Sharks were sampled in South Carolina waters for this written report, including 177 juveniles, 77 young of year, and eight adults (Table ane). All just one young of yr were captured in Bulls Bay and St. Helena Audio, while juveniles were captured in all sampled estuaries (Table ane). The δ¹⁵N signatures of historic period-0 Sandbar Sharks were significantly lower in summer–fall than in jump (Figure ii; Table 2) and did not decrease any further within the form of this written report, validating the choice of sampling approximately two months later most young of year are born (a July 15th cutoff) for reducing maternal contribution bias to age-0 Sandbar Sharks.

TABLE ii. Carbon and nitrogen stable isotopic signatures for Sandbar Shark muscle tissue from each life history phase. Values from all Sandbar Sharks, those collected before July 15th (bound), and those nerveless after July 15th (summer–fall) are shown.

FIGURE ii. Box plot of mean δ¹⁵N signature of age-0 Sandbar Sharks past capture month. The blackness squares represent the ways, the box dimensions represent the 25th–75th percentile ranges, and the whiskers show the tenth–90th percentile ranges. Boxes labeled with the aforementioned alphabetic character are non significantly different.

Initial multifactor ANOVA assay of summertime–fall Sandbar Sharks (Table A.1 in the appendix) indicated pregnant differences in δ¹⁵North betwixt estuaries (F = 8.6, P < 0.001) and no pregnant differences between historic period-classes (F = 2.01, P = 0.15). Assay of summer–fall Sandbar Sharks indicated significant differences in δ¹³C between historic period-classes (F = 8.2, P = 0.005), estuaries (F = 12.9, P < 0.005), month (F = eight.4, P < 0.005), and twelvemonth (F = 19.35, P < 0.005).

To account for the unbalanced sampling design (i.e., uneven numbers of young of yr between estuaries, unequal sampling of different estuaries in different months), each variable's effect on δ¹⁵N and δ¹³C was also analyzed with individual ANOVAs (Table A.ii in the appendix). When only young of year (due north = 53) and juveniles (n = 140) captured after July 15 (summer–fall) were analyzed separately to minimize potential maternal input or offshore feeding signals (Olin et al. 2011), ANOVA results indicated no significant differences for δ¹⁵N or δ¹³C signatures between years (Table A.2 in the appendix). When only summer–autumn juveniles or only summer–fall young of year were compared between estuaries, at that place were no significant differences in δ¹³C or δ¹⁵N between estuaries (Tabular array A.2 in the appendix). The pregnant differences betwixt estuaries appear to have been driven not past real isotopic differences between different estuaries, but by diff catch rates of young of twelvemonth between estuaries (Tabular array i), providing additional support to our decision to utilize multiple individual ANOVAs to analyze this dataset.

When all summer–fall Sandbar Sharks were pooled together from both years and all estuaries, δ¹⁵N and δ¹³C varied significantly between young of year and juveniles (Figure three), with college δ^xvN values (F = 6.4, P = 0.048) and more negative δ¹³C values (F = 62.9, P < 0.001) in juveniles than in young of yr (Tabular array A.2 in the appendix). Adults were excluded from this analysis due to depression sample size.

FIGURE 3. Mean δ¹⁵N and δ¹³C values (mistake bars are ±1 SE) of summer–fall Sandbar Sharks.

Juveniles had a larger δ¹⁵North range (four.5 versus 4.0), δ^xiiiC range (four.one versus 3.0), and total occupied niche area (14.1 versus vii.1) than immature of year (Effigy 4). Layman metrics of δ^fifteenN range, δ¹³C range, and full occupied niche area were very similar when comparing these metrics calculated for all Sandbar Sharks with those calculated for only summer–autumn Sandbar Sharks (well-nigh all of the outer points of the convex hull were summertime–fall sharks), and the results presented hither stand for all Sandbar Sharks. Adults were excluded from Layman metric analysis due to pocket-sized sample size. Regression analysis showed statistically significant effects of total length on both δ¹³C ratio (T = 4.18, P < 0.0005) and δ^xvNorth ratio (T = 3.6, P < 0.0005) (Effigy v).

FIGURE 4. Values of δ¹⁵N and δ¹³C from private muscle samples of all Sandbar Sharks. Polygons represent the total occupied niche surface area (and overlap) of all age-0 and juvenile Sandbar Sharks.

Effigy 5. Regression of δ¹⁵N (acme panel) and δ¹³C (bottom panel) by stretch total length for summertime–autumn Sandbar Sharks.

When using nutrition–tissue discrimination factors from Kim et al. (2012), historic period-0 Sandbar Sharks in Due south Carolina were assigned a trophic position of 3.8, while juveniles and adults were assigned a trophic position of 3.nine using the formula from Post (2002). The use of discrimination factors from Caut et al. (2009) resulted in trophic positions of 4.1 for immature of twelvemonth and four.3 for juveniles and adults, and the use of discrimination factors from Hussey et al. (2010) resulted in trophic position calculations of 4.2 for young of year and 4.3 for juveniles and adults. No difference in trophic position was found between using all Sandbar Sharks and only summer–autumn Sandbar Sharks, and then all samples were pooled for trophic analysis.

The potential casualty samples nerveless included 146 specimens of 21 species (Tabular array 3). All specimens of a unmarried species were pooled for prey assay to generate mean isotopic values for that species (Table 3). Benthic invertebrates identified as being important to the diet of age-0 Sandbar Sharks and squid Loligo sp. identified as existence of import to the diet of juveniles in Virginia by Ellis and Musick (2007) are approximately 1 trophic level (using nutrition–tissue discrimination factors from Kim et al. 2012) beneath age-0 Sandbar Sharks, suggesting that diets are similar between the regions (Figure 6).

FIGURE 6. Mean isotopic values of age-0 and juvenile Sandbar Sharks and co-occurring potential prey species. The squares represent Sandbar Sharks (CPJ are juveniles, CPY are immature of year), circles stand for invertebrates, triangles stand for elasmobranchs, and pluses stand for teleost fishes. Run across Table 3 for species abbreviations. Filled arrows indicate species identified equally beingness an of import part of the nutrition of historic period-0 Sandbar Sharks by Ellis and Musick 2007, empty arrows betoken of import prey species for juveniles identified by Ellis and Musick 2007, and crosshatched arrows betoken prey species identified as being important by Medved et al. 1985 (which did not distinguish by historic period-class).

Word

Our results suggest the presence of an ontogenetic diet shift between age-0 and juvenile Sandbar Sharks in S Carolina estuarine waters, indicated past differences in boilerplate δ¹⁵Northward and δ¹³C signatures between these two historic period-classes. This ontogenetic nutrition shift is consistent with young of year feeding mainly on small benthic animals (crustaceans such equally mantis shrimp and blue crab, elasmobranchs such as Atlantic Stingray, and teleosts such as Summertime Flounder) during the commencement year of life and expanding their diets to include additional pelagic animals (teleosts such as Atlantic Menhaden and invertebrates such every bit squid Loligo spp.) during the juvenile years. This diet shift, from mostly benthic invertebrates to more often than not pelagic teleosts, has been previously described from stomach content analyses of Sandbar Sharks in Hawaii (McElroy et al. 2006) and Virginia (Ellis and Musick 2007). Circumspection should exist utilized interpreting these information due to concerns virtually maternal contribution influencing the age-0 values and offshore feeding influencing the juvenile values, since the time for complete tissue isotopic turnover (Kim et al. 2012) exceeded the 2 months allowed by this study. Nevertheless, the many similarities between our conclusions and previous stomach-content-based Sandbar Shark diet analysis, including bear witness of an ontogenetic diet shift from benthic invertebrates to pelagic teleosts, give u.s.a. confidence in the robustness of our results.

Table 3. Carbon and nitrogen stable isotopic signatures of all South Carolina potential prey samples. Blueish crab size is carapace width, and ray size is disc width. All other sizes are total length.

The ontogenetic diet shift between summer–fall historic period-0 and juvenile Sandbar Sharks in this report was represented by a departure in δ¹⁵N of ∼0.three‰ and a divergence in δ¹³C of ∼1‰ between the two age-classes. Wells et al. (2008) studied juvenile and adult Blood-red Snapper and, due to a diet shift from zooplankton (chief consumers) to small teleosts and benthic crustaceans (secondary consumers), found a deviation of ∼1.3‰ in δ¹⁵N—as expected, a larger ontogenetic difference in δ¹⁵N than what nosotros observed in Sandbar Sharks in this written report because of a larger transition inside the food concatenation. The alter in δ^thirteenC that Wells et al. (2008) establish (∼1‰) is similar to changes observed in this study, and in both cases the predator changed feeding habitats within an ecosystem (benthic to pelagic for summer–autumn estuarine Sandbar Sharks, sandy bottom to reef for continental shelf Carmine Snapper). Estrada et al. (2006) plant a δ¹⁵N shift of ∼3‰ in the vertebrae of White Shark Carcharodon carcharias that was associated with a nutrition shift from teleosts to marine mammals that feed on teleosts. MacNeil et al. (2005) plant differences in δ¹⁵N comparable to those in this study (∼0.5‰) between liver and cartilage samples within individual Blue Sharks Prionace glauca and Common Thresher Sharks Alopias vulpinus, but larger δ¹⁵Northward differences (∼3‰) were found between liver and cartilage samples of Shortfin Makos. Blue and Thresher sharks switch diets between preferred teleost prey, a lesser nutrition alter than that of Shortfin Makos, which switch from preying on cephalopods to piscivorous Bluefish, and therefore accept a larger departure in δ^fifteenN signature than what was observed in this study. While regression analysis of total length past δ¹⁵Due north and by δ¹³C showed a significant effect of size on isotopic signature, the diet transition is non as abrupt as that found in Bluefin Tuna Thunnus thynnus by Graham et al. (2007).

South Carolina juvenile Sandbar Sharks had a larger δ¹⁵Northward range, δ¹³C range, and total occupied niche area than historic period-0 sharks, indicating a more diverse nutrition amidst juvenile individuals (Layman et al. 2007a). This is consistent with the increment in nutrition multifariousness observed in adult Sandbar Sharks in Hawaiian waters (McElroy et al. 2006). Additionally, the high degree of overlap in total occupied niche expanse between young of year and juveniles suggests that while Sandbar Sharks consume boosted prey species as they abound, older and larger juvenile sharks still swallow preferred young-of-year prey. This feeding strategy has been observed in multiple shark species (Grubbs 2010), such as the Tiger Shark Galeocerdo cuvier (Lowe et al. 1996), Broadnose Sevengill Shark Notorynchus cepedianus (Ebert 2002), Lemon Shark Negaprion brevirostris (Wetherbee et al. 1990), and Bonnethead Sphyrna tiburo (Bethea et al. 2007). The sample sizes between young of year and juveniles are significantly different, which could influence these calculations, just Vaudo and Heithaus (2011) performed a bootstrapping analysis and found asymptotes at a sample size of approximately 25–xxx, less than our smaller sample size, for several unlike coastal elasmobranch species.

As a higher full occupied niche expanse indicates a college diet latitude, the generalist feeding behavior of juvenile Sandbar Sharks observed in western N Atlantic estuaries (Ellis and Musick 2007) is reflected in the relatively loftier Layman metrics calculated in this study compared with other marine species. Layman metrics have been calculated for few other elasmobranch species to date. The δ¹⁵Due north range, δ^thirteenC range, and full occupied niche area calculations for the juvenile Sandbar Sharks in this report were larger than those for 9 of the 10 studied coastal elasmobranch species in Commonwealth of australia (Vaudo and Heithaus 2011). The Indo-Pacific Spotted Eagle Ray Aetobatus ocellatus, the largest batoid found in littoral Australian waters and the only local species with jaw morphology capable of crushing the shells of bivalve and gastropod prey, displayed higher Layman metric values than the Sandbar Sharks in our study (Vaudo and Heithaus 2011). Additionally, a marine piscivorous teleost in the littoral Bahamas, the Greyness Snapper Lutjanus griseus, has a total occupied niche area of 8.ix (Layman et al. 2007b), intermediate to that of historic period-0 (7.ane) and juvenile (14.1) Sandbar Sharks in Due south Carolina. It is of import to note that the present written report grouped together Sandbar Sharks from different estuaries while Vaudo and Heithaus (2011) sampled in a single arrangement, which may artificially increase the isotopic niche width of our samples if in that location are pregnant differences in baseline isotopic signatures betwixt estuaries sampled in this written report. Future calculations of Layman metrics for other marine predatory fishes will permit for interesting comparisons between species and habitats.

This report assigned age-0 Sandbar Sharks a mean trophic level of 3.viii and juvenile Sandbar Sharks a hateful trophic level of 3.9 using the formula from Mail service (2002) and nutrition–tissue discrimination factors from Kim et al. (2012). Adult Sandbar Sharks, which annually migrate between coastal and offshore waters, had a trophic level of three.9 (despite a small sample size [n = 8] that limits our confidence in these results), indicating a like diet to the juveniles. Based on seven Sandbar Shark nutrition studies included in a meta-analysis by Cortes (1999), four of which included adults (Wass 1973; Cliff et al. 1988; Stevens and McLaughlin 1991; Stillwell and Kohler 1993), Sandbar Sharks had a mean trophic level of four.1, not a significantly unlike value from our calculation of 3.8 (χ² = 0.9, P = 0.75). Trophic level can increase with increasing total length due to the ability of larger sharks to capture prey that smaller sharks cannot (Cortes 1999; Grubbs 2010), which explains the slightly lower trophic level observed in our study focusing on young of year and juveniles. The use of diet–tissue discrimination factors from Caut et al. (2009) and Hussey et al. (2010) resulted in very similar (but slightly higher) trophic position values, showing that, in this case, the trophic level estimates were relatively insensitive to diet–tissue discrimination factors.

Differences in the isotopic signature of Sandbar Sharks captured during April–June from that of summer–fall sharks (Table 2) potentially indicated the influence of maternal effects on the isotopic composition of newborn age-0 sharks (McMeans et al. 2009; Vaudo et al. 2010) and the influence of recent offshore feeding that afflicted the isotopic limerick of recently arrived juveniles in the months of May and June (Ulrich et al. 2007). Offshore food webs can have a less negative carbon signature than adjacent estuarine food webs (Leakey et al. 2008), with differences of up to four‰, which would influence the isotopic signatures of juvenile Sandbar Sharks that had recently been feeding offshore.

One time diff capture rates of young of year and juveniles were taken into account (past analyzing average isotopic signatures of young of year but and juveniles only), no significant differences were found between estuaries. Similar prey species were plant in each estuary, although local abundance can be variable (Bill Roumillat, SCDNR, personal communication). Between-estuary movements of age-0 and juvenile Sandbar Sharks in Virginia have been observed, just it is more mutual for Sandbar Sharks to remain within one estuary during a summer (Grubbs et al. 2007). Within South Carolina, tagging recaptures indicate seasonal fidelity to estuaries (Bryan Frazier, SCDNR, personal communication). No significant differences in δ¹⁵Northward or δ¹³C were found between sexes, which is consistent with the species' known life history, every bit age-0 and juvenile Sandbar Sharks are not known to spatially segregate based on sexual practice inside South Carolina estuaries (Ulrich et al. 2007).

The methods utilized in this study have important limitations that must be considered when interpreting these results. Dissimilar carbon signatures between juvenile and historic period-0 Sandbar Sharks may reflect a shift from benthic to pelagic feeding within an estuary, or they may reflect evidence of offshore feeding in juveniles despite our efforts to correct for this with a July 15th cutoff date. The apply of multiple single-factor ANOVAs, which were performed to correct for the unbalanced and opportunistic sampling regime, increases the chance of a type Two fault. Additionally, our determination to combine Sandbar Sharks and potential prey from different estuaries assumes that the baseline isotopic signature of these estuaries is very similar, which may or may not be the example. Additional sampling, which would accept ideally included principal producers and multiple individuals of each potential prey species from each estuary, would have resolved this just was not possible due to the logistical limitations of the written report. Single-tissue stable isotope analysis provides less information than analyses of multiple tissues, since different tissues have unlike turnover rates (MacNeil et al. 2005), though obtaining samples from normally used tissues such as liver and vertebrae unremarkably requires the sacrifice of animals. Finally, whenever possible, studies should be designed to obtain the data needed for precise statistical mixing models.

While lethal shark inquiry is sometimes necessary to obtain the data needed by fisheries managers, we agree with Heupel and Simpfendorfer (2010) and Hammerschlag and Sulikowski (2011) that nonlethal methods should be used whenever possible. No Sandbar Sharks were sacrificed for this project, and despite utilizing merely one tissue type (muscle), our results showed trends consistent with earlier lethal-sampling dietary research. Sharks have longer isotopic turnover rates than teleosts (Hesslein et al. 1993; Logan and Lutcavage 2010), and slow turnover rates have been observed in shark musculus tissue (MacNeil et al. 2005; Logan and Lutcavage 2010). Comparisons of stable isotope data with detailed tummy content analysis information, ideally obtained though gastric lavages, can provide complimentary dietary information merely are very labor intensive (Vaudo and Heithaus 2011). Our study is amid the beginning to detect an ontogenetic diet shift in a wild population of sharks using a nonlethal, single-tissue stable isotope analysis sample design.

Fisheries managers interested in creating an ecosystem-based fisheries direction program for the western North Atlantic Ocean Sandbar Shark population can incorporate data from this report. Sandbar Shark diet appears consistent betwixt estuaries, sexes, and years. A benthic-to-pelagic, crustacean-to-teleost ontogenetic diet shift similar to the shift documented in Virginia's and Hawaii's Sandbar Shark populations appears to as well occur in South Carolina'south population. Juvenile Sandbar Sharks have a wider diet breadth than age-0 sharks within South Carolina and have some of the highest values of diet latitude metrics e'er calculated in an elasmobranch, supporting the idea that they are generalist predators. Nosotros encourage hereafter muscle isotope studies of this blazon to reduce unnecessary lethal sampling of elasmobranchs and to provide bones dietary data to fisheries managers.

ACKNOWLEDGMENTS

The authors would similar to thank Mariah Boyle, Anabela Maia, Chuck Bangley, Jeremy Vaudo, Sora Kim, Colin Simpendorfer, Demian Chapman, R. Dean Grubbs, Bryan Franks, and Enric Cortes for their assistance with providing valuable data and multiple literature sources. Nosotros would also similar to thank Henry DaVega, Erin Levesque, and Jonathan Tucker from the SCDNR for their assistance with fieldwork. Bill Roumillat of the SCDNR provided prey samples and assisted with all stages of this project. Julie Higgins, Lisa May, and Kevin Beauchesne from the Hollings Marine Laboratory aided in the processing of stable isotope samples. This enquiry was supported by grant F-85-R4, F-77-6 of the Federal Assistance in Sport Fish Restoration program, the Cooperative States Shark Pupping and Nursery Habitat Survey, the State of South Carolina, and the Department of Biology of the College of Charleston, in addition to College of Charleston Kinesthesia Evolution and Department of Biology Research and Development grants to Gorka Sancho. The authors would as well like to thank ii anonymous reviewers whose feedback strengthened the manuscript. The handling of animals in this study was covered nether the College of Charleston IACUC permit # 2009-021. Sure commercial equipment, instruments, or materials are identified in this paper to specify fairly the experimental process. Such identification does not imply recommendation or endorsement past the National Institute of Standards and Technology, nor does it imply that the materials or equipment identified are necessarily the best available for the purpose. This is contribution 420 of the College of Charleston Graduate Program in Marine Biology and contribution 718 of the South Carolina Marine Resources Center.

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Source: https://www.tandfonline.com/doi/abs/10.1080/19425120.2014.920742

Bryan Stanley Charleston Institutes of Art Johnson and Wales

METHODS

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TABLE one. Biological and demographic data for all Sandbar Sharks sampled (total) and those from summer–fall (SF) months.

RESULTS

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TABLE ii. Carbon and nitrogen stable isotopic signatures for Sandbar Shark muscle tissue from each life history phase. Values from all Sandbar Sharks, those collected before July 15th (bound), and those nerveless after July 15th (summer–fall) are shown.

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Table 3. Carbon and nitrogen stable isotopic signatures of all South Carolina potential prey samples. Blueish crab size is carapace width, and ray size is disc width. All other sizes are total length.

ACKNOWLEDGMENTS

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