2012 SOUTHEASTERN NATURALIST 11(1):1–22 Prey Species of Bottlenose Dolphins (Tursiops truncatus) from South Carolina Waters S. Michelle Pate1,2,* and Wayne E. McFee3 Abstract - We describe the diet composition of Tursiops truncatus (Bottlenose Dolphin) from South Carolina waters. Stomach contents of 136 dolphins stranded dead between 2000 and 2006 were examined. Eighty-two dolphin stomachs contained food items and formed the basis for this study. The emphasis of this study was to compare the stomach contents of dolphins that bore evidence of human interaction but were otherwise healthy with those that appeared to die of natural causes. Forty-two prey species representing 24 families were identified. Dolphins fed predominantly on smaller-sized benthic and demersal fish species. Diets were primarily comprised of members of the family Sciaenidae, with Stellifer lanceolatus (Star Drum) being the most abundant species quantitatively. Lolliguncula brevis (Brief Squid) was the most frequently observed prey item. Overall, dolphins that appeared to have died from natural causes consumed similar species of fish and squid to those that exhibited signs of human interaction. This study represents the first quantitative analysis of prey species comprising the diet of Bottlenose Dolphins found in South Carolina waters. Introduction Defining the ecological role of marine predators such as Tursiops truncatus Montagu (Bottlenose Dolphin) can be difficult, as their aquatic existence often impedes direct observation of foraging behavior. Little information is available about the dietary habits of Bottlenose Dolphins in South Carolina. Young and Phillips (2002) developed an ecological model estimating the annual primary production required to support a small group of dolphins in a salt marsh creek ecosystem. Recks’ (2004) study of dietary history using blubber fatty-acid profiles from live free-ranging dolphins provide broad indices of food habits for Bottlenose Dolphins in the near-shore and estuarine waters around Charleston. Dietary studies on marine mammals traditionally have used dead stranded animals, but this might not accurately depict the dietary habits of healthy living populations because the possibility of poor health prior to stranding could bias the analysis (Selzer et al. 1986). If an animal was ill prior to stranding, it may have been unable to obtain food or fed on prey or prey sizes that do not represent normal foraging behavior. Stomach contents of animals that died an acute or sudden death (i.e., human-interaction cases) may be considered a better 1College of Charleston, 66 George Street, Charleston, SC 29424. 2Current address - South Carolina Department of Natural Resources, Marine Resources Research Institute, 217 Fort Johnson Road, Charleston, SC 29412. 3National Oceanic and Atmospheric Administration, National Ocean Service, Center for Coastal Environmental Health and Biomolecular Research, 219 Fort Johnson Road, Charleston, SC 29412. Corresponding author - PateS@dnr.sc.gov. 2 Southeastern Naturalist Vol. 11, No. 1 indicator of a “normal diet”. Although debate remains over the validity of using diet information from dead stranded animals, comparing dead stranded animals with animals known to have died from interactions with humans (e.g., fishery entanglements, boat strikes) could provide some insight into this problem. This study provides data on the feeding habits of Bottlenose Dolphins off the coast of South Carolina (Fig. 1) as determined through stomach content analysis. Accordingly, there were three primary objectives: 1) to quantitatively describe the diet of stranded Bottlenose Dolphins; 2) to determine if prey items consumed differed according to sex, age, and season, and between stranding locations; and 3) to determine if any significant differences existed in the dietary composition of dolphins that died from human interaction and dolphins that did not. Methods Sample collection Bottlenose Dolphins that stranded dead in the estuarine and nearshore (ocean) waters of South Carolina were inspected for signs of human interaction and classified into one of three categories: Non-human interaction (Non-HI), human interaction (HI), and cannot be determined (CBD). Dolphin death attributed to illness, disease, or natural causes were classified as Non-HI. Dolphin deaths due to fishery activities and boat strikes, or stranded dolphins exhibiting other signs (e.g., rope wounds, mutilation) associated with human activities were classified as HI (Geraci and Lounsbury 2005, Read Figure 1. Map of South Carolina coastline showing locations of non-human interaction and human interaction Bottlenose Dolphin strandings. 2012 S.M. Pate and W.E. McFee 3 and Murray 2000). Evidence of human interaction for dolphins in this study included: mutilation, parallel lacerations from boat propellers, presence of fishing gear (i.e., ingested or entangled), and marks suggestive of entanglement from other fishery interactions. Dolphin specimens were measured for total body length (taken from the tip of the upper jaw to the fluke notch; Hoffman 1991), and sex was determined when possible. Dolphins were also grouped as mature or immature. Maturity was determined via length, tooth aging, and/or the development of reproductive organs (Perrin and Reilly 1984). Male dolphins greater than 240 cm and female dolphins greater than 220 cm (Odell 1975) were considered sexually mature if gonads were not examined. Stomach analysis Whole stomachs (including forestomach, main, and pyloric chambers) were removed (in the field or in the laboratory), tied off at the esophageal and pyloric ends, placed in a labeled bag, and frozen at -20 °C pending further analysis. Each dolphin stomach was weighed (g) and whole, intact undigested prey items removed for identification and measurement. Remaining stomach contents were washed through a 1-mm sieve and hand sorted. The wet weight of the stomach contents was estimated by subtracting the weight of the empty stomach from the initial weight of the stomach with contents. Loose fish otoliths were stored dry. Identification of otoliths and fish bones was made using local reference collections and with assistance from the South Carolina Department of Natural Resources (SCDNR) Inshore Fisheries group (Charleston, SC). Published identification keys and pictorial guides were also used (Baremore and Bethea 2010, Campana 2004, Chao 1978, Gregory 1959, Mohsin 1981). Determination of left or right otoliths was based on the orientation of the sulcus acousticus. The number of intact fish, plus the greater number of either left or right sagittae indicated the minimum number of individual prey species present. When digestion of the sulcus prevented separation into either left or right sagittae, the total number of fish present was estimated by taking half the number of otoliths. Otoliths that were heavily digested or broken were classified as unidentified. Cephalopod beaks were stored in 70% ethanol and identified according to Clarke (1986) with the aid of a local reference collection. These were separated into upper and lower mandibles, and the greater count of either provided the estimated minimum number of individuals consumed. Counts of either shrimp rostra or telsons indicated the numbers of shrimp present. All prey items were identified to the lowest possible taxon. Dietary analysis Relative importance of individual prey items to total diet of each dolphin was determined using percent composition by number (%N) and percent frequency of occurrence (%F). These measures were also determined for stomachs grouped by sex, age, season, stranding location (ocean and estuarine) and stranding category (HI and Non-HI). Species richness (D) (the number of species per stomach) and 4 Southeastern Naturalist Vol. 11, No. 1 species diversity (H) using the Shannon Index (Krebs 1999) were also determined for dolphins classified as HI or Non-HI. Variation in the composition of prey items was evaluated according to sex, age, and season and between ocean and estuarine stranding locations. A comparison of diet composition between HI and Non-HI dolphins was made to assess the validity of using stranded dolphins to determine dietary habits of healthy dolphins. Hydrographic seasons were defined as: winter (December–February), spring (March–May), summer (June–August), and fall (September–November). Statistical analysis Non-parametric tests were used after rejecting the hypothesis of normality (Shapiro-Wilk test). All statistical analyses were conducted using JMP® statistical software (version 8.0.2.2; SAS Institute, Cary, NC). To determine the significance of diet variation between HI and Non-HI dolphins, a Mann- Whitney U (MWU) test was used to compare means for number of prey items (abundance), species richness, and wet weight of stomach contents. Contingency table analysis was used to compare observed frequencies of prey type (fish, squid, and shrimp) between Non-HI and HI dolphins and of specific prey species (≥2% composition by number) by dolphin sex and location between Non-HI and HI dolphins. To reconstruct prey measurements (length and weight) of species recovered from dolphin stomachs, linear regression equations of otolith lengths were derived from total length measurements of fresh prey specimens collected in Charleston, SC (Table 1). Measurements of excessively eroded or broken otoliths recovered from stomach contents were not included in the prey-size regression. Variation in the diet between male and female dolphins, between mature and immature dolphins, and between stranding locations for the total dolphin sample (HI and Non-HI combined) was examined using a Mann-Whitney U test comparing means for abundance, species richness, and wet weight of stomach contents. Differences in the abundance of prey species among seasons were investigated using a Kruskal-Wallis test. All results were significant at alpha level P > 0.05. Table 1. Regression equations relating otolith length (OL) to total length (TL) of fish and beak length (BL) to squid mantle length (ML) for six important species in the diet of Bottlenose Dolphins from South Carolina. Ranges of Length Weight Prey Items n Regression equation R2 (mm) (g) Stellifer lanceolatus 19 TL = 50.12 + 21.55 (OL) 0.780 109–128 12–28 Anchoa mitchilliA 16 SL = 12.1 + 21.4 (OL) 0.930 41–60 1–4 Leiostomus xanthurus 15 TL = -48.64 + 42.44 (OL) 0.996 46–220 2–141 Bairdiella chrysoura 16 TL = -4.2 + 37.15 (OL) 0.985 43–138 1–36 Micropogonius undulatus 29 TL = 8.85 + 27.44 (OL) 0.932 84–244 5–171 Lolliguncula brevis 11 ML = 11.07 + 48.03 (BL) 0.706 36–65 4–20 ARegression equation from Barros (1993), standard length (SL). 2012 S.M. Pate and W.E. McFee 5 Results Total dolphin sample composition Homogeneity in the dolphin sample was investigated using chi-square analysis for age, sex, and location variables. No significant differences were found when comparing the frequencies of prey types consumed; therefore, the pooling of data into groups based on age, sex, and location was considered appropriate as these variables should not introduce any bias (age: χ2 = 1.444, df = 2, P = 0.486; sex: χ2 = 4.667, df = 3, P = 0.198; location: χ2 = 5.033, df = 4, P = 0.284). Stomachs from 136 Bottlenose Dolphins collected between 2000 and 2006 were evaluated. One adult dolphin, determined to be of offshore ecotype based on genetic analysis and skull meristics (Hersh and Duffield 1990, Hoelzel et al. 1998, Mead and Potter 1995), and two adult specimens not sexed due to decomposition were excluded from analysis. Thirty neonate and 21 juvenile or adult dolphins (equivalent to 12% of HI and 23% of non-HI dolphins), whose stomachs contained only milk or were empty, were also excluded. The remaining 82 dolphin stomachs that contained food items (37 immature and 45 mature, 35 females and 47 males) were used to determine the relative importance of prey species consumed by Bottlenose Dolphins in South Carolina. Diet composition for stomachs containing food items The 82 dolphins whose stomachs contained evidence of food items were a mixture of HI and non-HI dolphins from ocean and estuarine regions. They fed predominantly on fish, which occurred in 90% (n = 74) of the stomachs examined. Squid alone was present in 10% of the dolphins (n = 8). The number of individual prey taxa found in individual stomachs ranged from 1 to 14, with a majority of the stomachs (77%) containing more than one type of prey species (mean = 4.90). Loose otoliths and cephalopod beaks recovered from the stomach contents numbered 14,852 and 141, respectively. The 82 dolphins fed on a minimum of 7851 individual prey items and a minimum of 42 different identified species of prey representing 24 different families (Tables 2, 3). Two-hundred twenty-six (226) otoliths and two cephalopod beaks were not identified, which could represent additional prey species consumed by dolphins in this study. Overall, important prey species in terms of abundance included Stellifer lanceolatus (Star Drum), Lolliguncula brevis (Brief Squid), Anchoa mitchilli (Bay Anchovy), and Leiostomus xanthurus (Spot). Brief Squid, contained in over half the stomachs (n = 47), were consumed most often. Prey species of the Sciaenidae family occurred in 76% of stomachs and represented 61% of prey items consumed. Dolphins consumed fishes ranging from 17 mm total length (TL) to 337 mm TL, as well as a 910-mm Mustelus canis (Smooth Dogfish; length estimated). The smallest fish species identified was Bay Anchovy with a mean TL of 44 mm. Mean TL of Star Drum, Bairdiella chrysoura (Silver Perch), Spot, and Micropogonius undulatus (Atlantic Croaker) consumed were 113 mm, 137 mm, 142 mm, and 210 mm, respectively. Brief Squid ranged in size from 17 to 65 mm mantle length (mean = 64). 6 Southeastern Naturalist Vol. 11, No. 1 Table 2. Percent composition by number (N) and percent frequency of occurrence (F) for prey items identified in the stomach contents of all Bottlenose Dolphins (n = 82), immature and mature male and female dolphins, and dolphins stranding in oceanic and estuarine waters of South Carolina between 2000 and 2006. The less than sign (<) denotes prey items less than 1% in numerical abundance. O = oceanic, E = estuarine. Common names and authorities for all species listed given in Table 3. All Immature Mature dolphins Females Males Females Males O E (n = 82) (n = 16) (n = 21) (n = 17) (n = 23) (n = 48) (n = 34) Prey items N F N F N F N F N F N F N F Bony fishes Sciaenidae Stellifer lanceolatus 40 44 56 38 19 48 36 35 30 43 22 32 54 29 Leiostomus xanthurus 10 37 6 50 3 24 12 29 23 30 19 26 2 26 Micropogonius undulatus 3 35 1 31 3 33 1 24 10 48 7 26 1 24 Bairdiella chrysoura 4 27 < 38 6 24 1 24 11 22 5 16 3 26 Cynoscion nothus 1 22 1 44 1 10 1 18 1 17 1 12 1 24 Larimus fasciatus 1 17 1 31 1 14 2 12 < 9 1 13 < 9 Cynoscion regalis 1 16 < 13 < 5 5 24 1 17 2 13 < 9 Menticirrhus americanus 1 10 1 13 < 5 < 12 1 13 1 7 < 6 Cynoscion spp. < 10 < 13 < 10 1 13 < 6 < 9 Menticirrhus spp. < 6 < 9 < 4 < 6 Cynoscion nebulosus < 6 < 6 < 5 < 6 < 9 < 1 < 9 Sciaenops ocellatus < 2 < 6 < 4 < 2 < 3 Pogonias cromis < 1 < 4 < 1 Sciaenid sp. < 1 3 6 < 1 Clupeidae Brevoortia tyrannus 2 26 2 44 1 33 < 6 < 13 4 16 1 24 Engraulidae Anchoa mitchilli 11 21 9 31 33 24 1 18 1 13 11 15 11 15 Anchoa hepsetus 4 16 < 31 13 24 < 12 3 4 4 11 3 12 Ophidiidae Cusk eel spp. 1 12 1 13 < 14 3 17 0 7 1 12 Mugilidae Mugil cephalus < 12 < 25 < 5 < 6 < 13 0 6 < 15 Triglidae Prionotus sp. 1 9 1 13 < 10 1 13 0 5 1 9 Sparidae Lagodon rhomboides < 7 < 13 1 6 2 13 1 5 < 6 Haemulidae Orthopristis chrysoptera < 6 < 13 < 5 < 9 < 4 < 6 Gadidae Urophycis sp. < 6 < 5 < 12 < 9 < 2 < 9 Trichiuridae Trichiurus lepiturus < 6 < 25 < 4 < 5 < 3 Bothidae Paralichthys dentatus < 7 < 13 < 5 < 9 < 4 < 9 Paralichthys lethostigma < 2 < 4 < 2 Paralichthys sp. < 1 < 1 Batrachoididae Opsanus tau 2 12 2 19 4 10 < 6 < 17 < 4 3 21 Porichthys plectrodon < 4 < 6 < 5 < 4 < 4 2012 S.M. Pate and W.E. McFee 7 There were 131 undigested fish representing ten species recovered from the stomachs of thirteen dolphins. The fish recovered included Brevoortia tyrannus (Atlantic Menhaden), Peprilus triacanthus (Butterfish), Menticirrhus spp., Paralichthys dentatus (Summer Flounder), Spot, Porichthys plectrodon (Atlantic Midshipman), Atlantic Croaker, Opsanus tau (Oyster Toadfish), Menticirrhus americanus (Southern Kingfish), and Mugil cephalus (Striped Mullet). The largest proportion of whole fish remains recovered ranged from 80–119 mm TL. The largest undigested teleost fish was an Oyster Toadfish at 291 mm TL, followed Table 2, continued. All Immature Mature dolphins Females Males Females Males O E (n = 82) (n = 16) (n = 21) (n = 17) (n = 23) (n = 48) (n = 34) Prey items N F N F N F N F N F N F N F Synodontidae Synodus foetens < 5 < 6 1 6 1 4 1 4 < 3 Anguillidae Anguilla rostrata < 5 2 10 < 6 < 4 < 4 < 3 Ophichthidae Myrophis punctatus < 1 < 6 < 1 Ophichthus gomesi < 1 < 5 Elopidae Elops saurus < 2 < 6 < 4 < 2 Serranidae Centropristis striata < 1 < 6 Centropristis philadelphica < 1 < 6 Stromateidae Peprilus triacanthus < 1 < 1 Arridae Catfish sp. < 1 < 4 < 1 Carangidae Selene setapinnis < 1 < 6 Blenniidae Hypsoblennius hentzi < 1 < 6 Unidentified fish Unidentified fish spp. 3 45 1 50 3 43 < 24 7 52 4 29 2 38 Cartilaginous fish Triakidae Mustelus canis < 1 < 1 Cephalopods Lolliginidae Lolliguncula brevis 13 56 15 75 6 43 32 59 5 52 9 33 16 56 Unidentified squid sp. < 1 < 6 < 3 Crustaceans Penaeidae Litopenaeus setiferus 1 16 1 25 2 14 < 12 < 9 2 12 1 9 Penaeus aztecus < 2 < 13 < 6 Unidentified shrimp sp. < 7 < 10 < 18 < 4 < 4 < 9 Portunidae Portunus sayi < 1 < 1 8 Southeastern Naturalist Vol. 11, No. 1 Table 3. Scientific names with authorities and common names for fish species identified as prey items in the stomachs of Bottlenose Dolphins examined in this study. Prey items Common name Prey items Common name Bony fishes Porichthys plectrodon Jordan & Gilbert Atlantic Midshipman Sciaenidae Synodontidae Stellifer lanceolatus Holbrook Star Drum Synodus foetens L. Inshore Lizardfish Leiostomus xanthurus Lacepède Spot Stromateidae Micropogonius undulatus L. Atlantic Croaker Peprilus triacanthus Peck Atlantic Butterfish Bairdiella chrysoura Lacepède Silver Perch Anguillidae Cynoscion nothus Holbrook Silver Seatrout Anguilla rostrata Lesueur American Eel Larimus fasciatus Holbrook Banded Drum Ophichthidae Cynoscion regalis Bloch & Schneider Weakfish Myrophis punctatus Lütken Speckled Worm Eel Menticirrhus americanus L. Southern Kingfish Ophichthus gomesi Castelnau Shrimp Eel Cynoscion nebulosus Cuvier Spotted Seatrout Elopidae Sciaenops ocellatus L. Red Drum Elops saurus L. Ladyfish Pogonias cromis L. Black Drum Serranidae Clupeidae Centropristis striata L. Black Sea Bass Brevoortia tyrannus Latrobe Atlantic Menhaden Centropristis philadelphica L. Rock Sea Bass Engraulidae Carangidae Anchoa mitchilli Valenciennes Bay Anchovy Selene setapinnis Mitchill Moonfish Anchoa hepsetus L. Striped Anchovy Blenniidae Mugilidae Hypsoblennius hentzi Lesueur Feather Blenny Mugil cephalus L. Striped Mullet Cartilaginous fish Sparidae Triakidae Lagodon rhomboides L. Pinfish Mustelus canis Mitchill Smooth Dogfish Haemulidae Cephalopods Orthopristis chrysoptera L. Pigfish Lolliginidae Trichiuridae Lolliguncula brevis Blainville Brief Squid Trichiurus lepiturus L. Cutlassfish Crustaceans Bothidae Penaeidae Paralichthys dentatus L. Summer Flounder Litopenaeus setiferus L. Northern White Shrimp Paralichthys lethostigma Jordan & Gilbert Southern Flounder Penaeus aztecus Ives Northern Brown Shrimp Batrachoididae Portunidae Opsanus tau L. Oyster Toadfish Portunus sayi Gibbs Sargassum Crab 2012 S.M. Pate and W.E. McFee 9 by a Southern Kingfish at 227 mm TL. Eighty-five (64.9%) of the 131 whole fish recovered from the stomachs were Atlantic Menhaden. Non-HI and HI dolphin diet comparison Fifteen dolphins were categorized as HI for this analysis: five stranded in the oceanic region and ten within the estuarine region. Of the remaining sixty-seven dolphins that had food items present in their stomachs, the cause of death for five dolphin carcasses could not be deemed direct results of observed human interaction and were classified as CBD. Therefore, 62 dolphins containing food items were considered non-HI: 39 stranded in the oceanic region and 23 in the estuarine region. The smaller HI sample size prevented examination by season and age; therefore, evaluation of differences in prey items was restricted to sex and stranding location. Although the differences were not found to be statistically significant (Z = 1.872, P = 0.061), mean number of items consumed by HI dolphins was 86 (range: 2–389) whereas Non-HI dolphins consumed an average of 68 items (range: 1–473). HI dolphins on average consumed a more diverse diet, with an average of 6.20 ± 4.35 SD different prey taxa per stomach compared to 4.47 ± 3.74 SD for Non-HI dolphins (Z = 1.366, P = 0.172). The mean stomach wet weight among HI dolphins was 555 g, with a range of 18–2430 g, and for non-HI dolphins the mean was 278 g, with a range of 0–2970 g (Z = 1.427, P = 0.154). Richness (D) was 1.03 for HI dolphin species, and 0.60 for non-HI species. Species diversity (H) was 2.25 for HI dolphins and 2.46 for non-HI dolphins. The prey composition of the stomach contents was analyzed according to how frequently each prey type (fish, shrimp, and squid) or any combination of the three occurred. Fish alone or in combination with other prey types accounted for 90% of the samples in non-HI dolphins and 87% of samples in HI dolphins. Shrimp alone was never observed in any specimens, and squid alone occurred in 10% and 13% of the non-HI and HI samples, respectively. The stomach contents of non-HI dolphins revealed a predominance of fish alone, but no significant difference was found between HI and non-HI dolphins for the frequency of occurrence of fish (χ2 [n = 77] = 0.173, P = 0.677) or squid (χ2 [n = 77] = 1.104, P = 0.293). However, shrimp was found to occur more significantly in the HI dolphins (χ2 [n = 77] = 4.149, P < 0.042). Non-HI female dolphins consumed ten different species, while HI females consumed individuals from 5 different species (Table 4). Brief Squid, accounting for half the diet composition by number, dominated the diet of HI female dolphins. HI female dolphins also consumed Star Drum, Atlantic Menhaden, Cynoscion nothus (Silver Seatrout), and Spot to a lesser extent. Despite the abundance of a single species in the diet of HI females, there were no significant differences in the frequency of occurrence for the ten species evaluated between non-HI and HI females (contingency table analysis, P > 0.05). Non-HI males consumed eight prey species (≥2% by number), while HI male dolphins consumed nine species. Bay Anchovy and Oyster Toadfish were consumed significantly more often by HI male dolphins (χ2 [n = 44] = 5.246, P < 0.022; χ2 [n = 44] = 4.728, P < 0.030). 10 Southeastern Naturalist Vol. 11, No. 1 Table 4. The percent composition by number (N) and percent frequency of occurrence (F) for prey items recovered from the stomach contents of non-human interaction (non-HI) and human interaction (HI) Bottlenose Dolphins stranded in waters of South Carolina collected between 2000 and 2006. Less than sign (<) denotes prey item less than 1% composition by number. Prey items measuring less than 2% composition by number for all categories not presented in table. Non-HI HI Oceanic Estuarine Male Female Male Female Non-HI HI Non-HI HI (n = 36) (n = 26) (n = 8) (n = 7) (n = 39) (n = 5) (n = 23) (n = 10) Prey Items N F N F N F N F N F N F N F N F Bony Fishes Sciaenidae Stellifer lanceolatus 21 42 21 38 32 63 20 29 23 54 31 40 15 17 29 50 Leiostomus xanthurus 15 28 16 42 10 63 2 14 20 44 18 40 3 22 6 40 Micropogonius undulatus 9 42 3 31 1 25 0 14 8 49 0 0 2 17 1 30 Bairdiella chrysoura 7 19 1 31 10 38 1 29 6 31 0 0 1 13 9 50 Cynoscion nothus 1 14 1 27 1 38 3 29 1 23 0 0 1 13 1 50 Larimus fasciatus 1 14 2 19 0 25 0 0 1 21 1 40 2 9 0 0 Cynoscion regalis 1 17 2 23 0 13 0 0 2 23 3 20 < 13 0 0 Menticirrhus americanus 1 8 2 12 0 25 0 0 2 13 < 20 < 4 < 10 Unidentified Sciaenidae 0 0 2 4 0 0 0 0 1 3 0 0 0 0 0 0 Clupeidae Brevoortia tyrannus 3 25 3 19 2 50 9 14 4 26 8 40 1 17 3 30 Engraulidae Anchoa mitchilli 16 14 1 27 17 50 0 0 13 28 1 20 < 4 16 30 Anchoa hepsetus 12 14 1 15 0 13 0 14 5 18 < 20 12 9 < 10 Ophidiidae Cusk eel spp. < 11 1 8 5 38 0 0 < 10 2 20 2 9 4 20 2012 S.M. Pate and W.E. McFee 11 Table 4, continued. T Non-HI HI Oceanic Estuarine Male Female Male Female Non-HI HI Non-HI HI (n = 36) (n = 26) (n = 8) (n = 7) (n = 39) (n = 5) (n = 23) (n = 10) Prey Items N F N F N F N F N F N F N F N F Triglidae Prionotus spp. < 8 2 4 0 13 0 0 < 8 0 0 3 4 < 10 Batrachoididae Opsanus tau < 8 4 12 7 38 1 14 1 8 0 0 6 13 6 40 Synodontidae Synodus foetens < 3 < 4 1 13 0 14 1 5 3 20 0 0 < 10 Unidentified fish spp. 4 50 3 35 6 75 1 43 4 51 2 60 1 35 6 60 Cephalopods Lolliginidae Lolliguncula brevis 7 47 34 62 2 63 58 71 8 56 15 60 48 48 13 70 Crustaceans Penaeidae Litopenaeus setiferus 1 11 1 15 4 38 0 14 1 21 11 40 1 0 1 20 12 Southeastern Naturalist Vol. 11, No. 1 The percent composition by number and percent frequency of prey items recovered from Non-HI and HI dolphins that stranded in both the oceanic and estuarine regions of South Carolina are listed in Table 4. Non-HI dolphins stranding in the oceanic region consumed prey (>2% by number) belonging to 10 species: Star Drum, Spot, Bay Anchovy, Brief Squid, Silver Perch, Atlantic Croaker, Atlantic Menhaden, Anchoa hepsetus (Striped Anchovy), Cynoscion regalis (Weakfish), and Southern Kingfish. HI dolphins also consumed Star Drum, Spot, Brief Squid, shrimp, Atlantic Menhaden, Synodus foetens (Inshore Lizardfish), Weakfish, and Ophidiidae spp. (cusk eels). The diet of both non-HI and HI dolphins stranding in the estuarine region included Star Drum, Bay Anchovy, Spot, and Brief Squid among others. Brief Squid dominated the diet for non-HI dolphins in number at 48%, yet the observed frequency of occurrence of squid between HI and non-HI dolphins was not statistically significant (χ2 [n = 33] = 1.382, P > 0.240). Silver Perch and Bay Anchovy occurred significantly more frequently in the diet of HI dolphins stranded in the estuarine region (χ2 [n = 33] = 5.183, P < 0.023; χ2 [n = 33] = 4.306, P < 0.038). Differences in diet according to dolphin sex and maturity for overall sample Combining the HI and non-HI dolphins specimens together allowed comparisons in diet to be made for the overall sample (n = 82) between dolphin sex and maturity. Female dolphins consumed a greater diversity of prey taxa (mean = 5.14 ± 4.1) than males (mean = 4.74 ± 3.9) and a greater abundance of prey items (mean = 124 ± 375) than males (mean = 74 ± 115). The average stomach content wet weight was 368 g for females and 356 g for males. However, the differences between the averages for taxa, prey items, and wet weight between males and females were not statistically significant (taxa: Z = 0.464, P = 0.643; prey items: Z = 0.525, P = 0.599; wet weight: Z = 0.217, P = 0.828). Among maturity stages, sexually mature and immature males consumed nearly the same average number of prey items (means = 75 and 74, respectively). Sexually immature females consumed an average of 220 prey items, and mature females consumed an average of 44 items. The diet of immature female dolphins was dominated in number by Star Drum (56%). However, Brief Squid was observed most frequently at 75%, with Star Drum only occurring in 38% of the samples. There were no significant differences in the averages evaluated for taxa, prey items, and wet weight between immature and mature dolphins (taxa: Z = 0.541, P = 0.588; prey items: Z = 0.420, P = 0.675; wet weight: Z = 0.022, P = 0.951). The diet composition by number and percent frequency of occurrence for select prey species consumed by immature and mature male and female Bottlenose Dolphins are listed in Table 2. Over half of the prey items consumed by mature females in number consisted of Star Drum (36%) and Brief Squid (32%). Star Drum (56%) was the most consumed prey item in number for the immature females’ diet. The diet of mature males was composed, by number, of eight different prey species (87%), whereas immature males contained ten 2012 S.M. Pate and W.E. McFee 13 (89%). Mature males consumed Star Drum, Spot, Silver Perch, and Atlantic Croaker. Immature males consumed Bay Anchovy, Star Drum, and Striped Anchovy. Brief Squid was the most frequently observed prey item for all sex and maturity classes with the exception of immature males. In immature males, Star Drum was observed most often. Differences in diet according to stranding location for overall sample The diet composition by number of dolphins stranded in the oceanic region primarily consisted of Star Drum (22%), Spot (19%), and Bay Anchovy (11%). Dolphins in this region consumed an average of 45 prey items, consisting of an average of 5.40 ± 3.7 prey taxa, with a mean wet weight of 424 grams. More than half of the estuarine dolphin diet composition consisted of Star Drum (54%), followed by Brief Squid (16%). Estuarine dolphins consumed an average of 128 prey items, consisting of an average of 4.21 ± 4.2 prey taxa with a mean wet weight of 293 grams. Brief Squid was the most frequently observed prey item in both the oceanic (56%) and estuarine regions (33%) (Table 2). Seasonal differences in diet Nineteen Bottlenose Dolphins stranded during winter, 17 during spring, and 23 dolphins each during the summer and fall. Star Drum was observed in stomachs in all four seasons, but was most abundant during winter and least abundant during summer (Fig. 2). Brief Squid was the most abundant prey in the spring and was observed most frequently in every season except winter. Bay Anchovies were consumed in every season except spring. Spot was consumed in every season except winter and was the only species significantly abundant in the dolphin diet (Kruskal-Wallis, Fall: H = 9.51, P > 0.023). Atlantic Croaker, Striped Anchovy, and Atlantic Menhaden were only consumed in the summer and fall. More species were observed or consumed during fall (n = 11) than winter (n = 4), with spring and summer having intermediate abundances. Discussion Human interaction dolphins The inherent problems with the use of stomach content analysis for determining dietary habits have been reviewed in various papers (Jobling and Breiby 1986, Pierce and Boyle 1991) and researchers suggest that the stomach contents of dolphins exhibiting signs of human interaction would better represent the diet of healthy individuals. Previous studies on Bottlenose dolphin stomach contents throughout the southeastern United States found no qualitative differences in the diet of stranded dolphins that died as a result of natural and anthropogenic causes (Barros 1993, Barros and Odell 1990, Mead and Potter 1990). An objective of this study was to assess the validity of using stranded dolphins to determine the dietary habits of dolphins through a statistical comparison of the diets of dolphins whose deaths were not of anthropogenic origin (presumed diseased) and dolphins that died as a result of human interaction (presumed healthy based on histopathology results). 14 Southeastern Naturalist Vol. 11, No. 1 Results of the evaluation between the non-HI and HI Bottlenose Dolphins in the waters of South Carolina indicated that both groups of dolphins consume a similar diet of fish, cephalopods, and crustaceans. These results are consistent with previous analysis of stomach contents of Bottlenose Dolphins in the southeastern United States. However, shrimp occurred significantly more often in the HI group, indicating those dolphins could be incidentally ingesting shrimp more often than non-HI dolphins while targeting by-catch species and prey items stirred up during the trawling process. Overall dietary habits of dolphins in South Carolina Bottlenose Dolphins stranded in South Carolina waters were primarily piscivorous, consuming a variety of smaller-sized benthic and demersal coastal inshore fish species. The most abundant family of fish consumed in this study was the Sciaenidae, typically found in estuaries, in muddy bays, and near shallow banks. Star Drum numerically dominated the dietary composition of dolphin stomach contents. This small bottom-dwelling fish is the most abundant marine fish in the coastal waters of South Carolina (Bearden 1964), and the mean size consumed by dolphins in this study was 113 mm, equivalent to a juvenile or one-year-old fish of this species (Shealy et al. 1974). Star Drum typically spawns in the late spring and early summer, with a peak spawning Figure 2. Important prey items in terms of percent composition by number (for species greater than 2%) recovered from the stomach contents of stranded Bottlenose Dolphins in South Carolina according to season. All prey species representing less than 2% composition by number were grouped collectively in the “other” category. 2012 S.M. Pate and W.E. McFee 15 period in July (Shealy et al. 1974). Unlike many fish species, Star Drum appear to exhibit no spawning migration, as both juveniles and adult fish are present in estuaries during the spawning season (Shealy et al. 1974). In this study, Star Drum was consumed throughout the year in varying quantities, reflecting the seasonal abundance, prey availability, and seasonal pattern in sound production. The distribution of Star Drum along the Atlantic coastline varies, but they most often occur from North Carolina to Northeast Florida, which may explain why this species is not consumed to a greater extent by dolphins further south or in the Gulf States. Bottlenose Dolphins are diverse in their consumption of various species (42 different species consumed in this study alone) yet preferences were apparent. Sciaenids, which dolphins in this study consumed abundantly, are highly soniferous (Ramcharitar et al. 2006) and are prevalent in the nearshore waters off the south Atlantic coast (SCDNR SEAMAP 2000). Additional soniferous fishes consumed to a lesser extent by dolphins in this study included members of the family Batrachoididae (Oyster Toadfish and Atlantic Midshipman; Fish and Mowbray 1970, Gray and Winn 1961) and Ophidiidae (cusk eels; Mann et al. 1997, Sprague and Luczkovich 2001). Previous stomach content studies in the southeastern United States (Barros 1993, Barros and Odell 1990, Gannon 2003, Gannon and Waples 2004) demonstrated that soniferous fishes, especially Sciaenids, also dominated the dolphins’ diet. However, dolphins did not appear to consume soniferous fish at those times when they would be most actively producing sounds (i.e., spawning). Gannon (2003) also found this to be true, and suggested that members of the family Sciaenidae might produce vocalizations not associated with spawning, but nevertheless detectable by dolphins (Gannon and Waples 2004). Barros and Odell (1990) first theorized that Bottlenose Dolphins employ passive listening while foraging to explain the consumption of sound-producing fish. Gannon et al. (2005) later tested this theory, providing experimental evidence that dolphins responded to recorded calls of prey fish, changing their travel direction and rate of echolocation to orient themselves toward the source of the sounds and Gannon and Taylor (2007) documented that Atlantic Croaker produced sound outside of the spawning season. Berens McCabe et al. (2010) found wild resident Bottlenose Dolphins occupying an inshore coastal habitat selected for soniferous prey, lending further support to the passive-listening foraging hypothesis. Dolphins in the present study occupied both coastal inshore and open coastal habitats which likely require the use of multiple foraging techniques including passive listening and would account for the variety of fish species consumed overall. Striped Mullet has long been considered a common prey item for Bottlenose Dolphins (Barros and Odell 1990, Barros and Wells 1998, Caldwell and Caldwell 1972, Gunter 1942, Shane 1990), and the near absence of this species in the dolphin samples was notable. Mullet are commonly found in coastal inshore waters year round, but spawn offshore and can tolerate a wide salinity range in South Carolina (McDonough et al. 2003). Dolphins have been observed capturing mullet while “strand feeding” on intertidal creek banks in South Carolina (Petricig 1995, Zolman 1996). Mullet jump out of water when 16 Southeastern Naturalist Vol. 11, No. 1 chased by predators, and this increased visibility may lead observers to overestimate the amount of mullet actually fed on by dolphins (Barros and Odell 1990). Berens McCabe et al. (2010) also found no quantitative evidence for the hypothesis that Bottlenose Dolphins select for Striped Mullet. Blubber fatty acid analysis on living dolphin populations in South Carolina (Recks 2004) found evidence that mullet were consumed, but dolphins occupying the North Edisto River (just South of Charleston, SC) specifically appeared to consume more mullet than dolphins of other Charleston waters. Recks (2004) conceded that the unique signature of mullet that contributes to its ease of detection in fatty acid analysis could cause it to be overestimated in its importance to the dolphin diet. However, results from the present study showed that Striped Mullet contributed a very small amount (less than 1%) to the diet of dolphins in South Carolina. Mead and Potter (1990) found no evidence of mullet in Bottlenose Dolphins stranded in North Carolina, Virginia, and Maryland, and less than 1% was observed in stomachs analyzed by Gannon (2003) from North Carolina. Results from the Indian River Lagoon in Florida indicated a small number of mullet consumed by dolphins there (Barros 1993). Sex and maturity Results of the present study on Bottlenose Dolphins indicated there was a dietary difference by sex and maturity. The diet of immature males showed a dominance of schooling fish species, with almost half of prey items consisting of anchovies. This targeting of schooling fish may be the response of inexperienced hunters attracted to prey items that may be easier to catch. These large numbers of anchovies present could be secondary ingestion from another fish species consumed; however, we would anticipate seeing large numbers of otoliths from higher trophic level fish also present in the stomach. Brief Squid was the most frequent prey species of all dolphins with the exception of immature males. Although differences were not significant, there appeared to be a trend for female dolphins to consume Brief Squid, especially among reproductively mature females. Gannon (2003) found similar results with mature female Bottlenose Dolphins in North Carolina. Female Stenella attenuata (Gray) (Pantropical Spotted Dolphin) also consumed more squid in a study by Robertson and Chivers (1997). Cockcroft and Ross (1990) found lactating Bottlenose Dolphins consumed more cephalopods than non-lactating females. Bernard and Hohn (1989) found female Spotted Dolphins consumed more fish during lactation, while pregnant females consumed more squid. The authors conceded that dietary results for lactating females might not be the norm, referencing a larger sample of Spotted Dolphins from the same area whose dominant food item was squid. Females could be consuming squid because of higher caloric content required for reproduction or lactation or because of habitat preferences. Additionally, the optimal foraging theory (MacArthur and Pianka 1966) predicts that an animal will behave in a way that maximizes its caloric intake while minimizing its effort including behavior such as avoidance of predators. The increased energetic requirements dictate that these animals will meet the caloric demands 2012 S.M. Pate and W.E. McFee 17 by consuming more of their normal prey while supplementing their diet with the next best species available. Without more information on the caloric value of squid as compared to fish species, it is difficult to interpret the consumption trend of squid by female dolphins in this study. Stranding locations Dietary differences among the oceanic and estuarine dolphins appeared to reflect different prey availability in the habitats they occupy. Residence patterns have been established for Bottlenose Dolphins occupying a least one estuarine area in South Carolina (Zolman 2002). Distribution patterns and diet composition of Bottlenose Dolphins in estuarine areas suggest that dolphins forage on the most prevalent teleost fish species occurring in the habitat they routinely occupy, such as Star Drum. The prey composition of the oceanic region was compared with results of the dietary studies on Bottlenose Dolphins that inhabited similar habitat along the coast of North Carolina (Gannon and Waples 2004) in an effort to assist with the stock differentiation of Bottlenose Dolphins occupying nearshore South Carolina waters. The diet composition of dolphins that stranded in the oceanic region of this study was comprised mainly of Atlantic Croaker, Spot, and Striped Anchovy. Bottlenose Dolphins stranded on ocean beaches of North Carolina consumed Weakfish, Atlantic Croaker, Spot, inshore squid, and Striped Anchovy, varying in abundance throughout year (Gannon 2003, Gannon and Waples 2004). Mead and Potter’s (1990) study that included samples from North Carolina, also identified Weakfish, Atlantic Croaker, and Spot as primary dietary components. Although Weakfish was a primary dietary component of oceanic dolphins in North Carolina, dolphins in the coastal region of this study consumed less than 2%. This smaller quantity observed in South Carolina dolphins is likely due to the fish’s distribution patterns along the Eastern US coastline, as Weakfish congregate in much larger numbers off North Carolina and points north. Seasonality Bottlenose Dolphins’ diets appeared to reflect seasonal fluctuations in available prey. A similar seasonal trend in the diet of living dolphins in the estuarine and near-shore coastal waters around Charleston, SC, was also detected using blubber fatty acid analysis (Recks 2004). In this study, Star Drum was found in all four seasons, but was the most dominant prey in winter (67%) and the lowest in the summer (11%). Star Drum is the most abundant demersal fish species occurring in estuarine waters (Wenner et al. 1984), remaining in estuaries when many other fish species migrate offshore during cooler months, thereby restricting dolphins with little other choice for food resources inside estuaries. Spot was consumed significantly more in the fall by Bottlenose Dolphins in this study. Recks’ (2004) study also found Spot to be consumed significantly more during summer and fall. Spot are an estuarine-dependent species abundantly occurring in South Carolina inshore waters, second only to Star Drum. These fish are considered year-round residents of South Carolina waters (Dawson 18 Southeastern Naturalist Vol. 11, No. 1 1958, Keiser 1976). Adult fish exhibit seasonal shifts in distribution between the coastal ocean and estuary with young-of-the-year remaining in estuaries during their first winter. Shrimp trawl surveys show an abundance of Spot caught during fall months during which large schools of migrating fish appear along South Carolina beaches. Larger Spot spawn offshore during winter months, accounting for its absence in the winter dolphin samples (Dawson 1958). Fishery interactions Bottlenose Dolphins have frequently been sighted following and feeding in association with shrimp trawlers (Caldwell and Caldwell 1972; Corkeron et al. 1990; Fertl 1994; Gunter 1942, 1951; Leatherwood 1975). Shrimp is the most valuable fishery in the near-shore coastal waters of South Carolina (SCDNR 2006). Its season extends from approximately May through January in the coastal waters from Georgetown, SC to the Georgia/South Carolina border (Keiser 1976). During a long-term photo-identification study of Bottlenose Dolphins near Charleston, twenty percent of the dolphin sightings between June and November showed association with shrimp trawlers (Speakman et al. 2006). While a wide variety of species are caught incidentally in the fishery trawls, the Sciaenids were the predominant family of fishes in the composition (representing approximately 60% of the catch) of discarded “trash” fish (Keiser 1976) and were the family of fishes most consumed by dolphins in this study. Bay Anchovy, Brief Squid, Star Drum, Silver Perch, Weakfish, Spot, Atlantic Croaker, and Southern Kingfish are all species considered by-catch of local shrimp trawlers (Keiser 1976) and are among the species caught most prevalently in independent-fishery surveys along the South Atlantic Bight (SCDNR SEAMAP). These individual species were among the most-consumed prey items in the diets of Bottlenose Dolphins in South Carolina, indicating that dolphins may be taking advantage of the food resource provided by trawling efforts. In this study, shrimp was consumed more often by dolphins that stranded in the oceanic region where shrimp trawling occurs. Recks (2004) found the fatty acid profiles of dolphins sampled behind shrimp boats were distinct from estuarine dolphins. Although dolphins in this study consumed shrimp, the amount recovered from the stomach contents in relation to the proportion of fish was small. The large proportion of by-catch consumed would suggest that the dolphins were not targeting shrimp. Rather, it would suggest they were indirectly consuming some shrimp while targeting fish caught in the nets of the shrimp trawlers. This study provided the first comprehensive characterization of the diet of Bottlenose Dolphins collected in the waters of South Carolina. Although the results of this study cannot be used to provide conclusive proof that the prey items consumed by stranded dolphins are representative of a Bottlenose Dolphin population at large, it does lend support to that hypothesis. The wide range of species identified from stomach remains indicate food habits that incorporate a variety of prey known to inhabit the estuarine and coastal waters of South Carolina. The prey items consumed by Bottlenose Dolphins are also fish species consumed by 2012 S.M. Pate and W.E. McFee 19 humans and some dolphins have been found to have high contaminant loads. From a human health aspect, knowing what these animals eat may also assist in determining dolphin forage areas, and knowledge of this forage area may be important when analyzing unusual mortality events. Investigations of unusual mortality events can serve as indicators of ocean health and lead to further potential implications on human health. Acknowledgments The lead author gratefully acknowledges the assistance provided by L. Burdett, J.W.B. Powell, M.A. Recks, L.B. Rust, J.A. Stephen, and especially that of W.A. Roumillat. The authors thank the South Carolina Marine Mammal Stranding Network, and the SCDNR Inshore Fisheries and SEAMAP groups. The authors also thank W.A. Roumillat, P. Fair, G. Seaborn. and E. Zolman for comments on earlier versions of this manuscript. This research was made possible through NOAA’s responsibility under the Marine Mammal Health and Stranding Response Act, Section 109(h) of the Marine Mammal Protection Act. Disclaimer: This publication does not constitute an endorsement of any commercial product or intend to be an opinion beyond scientific or other results obtained by the National Oceanic and Atmospheric Administration (NOAA). No reference shall be made to NOAA, or this publication furnished by NOAA, to any advertising or sales promotion which would indicate or imply that NOAA recommends or endorses any proprietary product mentioned herein, or which has as its purpose an interest to cause the advertised product to be used or purchased because of this publication. Literature Cited Baremore, I.E., and D.N. Bethea. 2010. A guide to otoliths from fishes of the Gulf of Mexico. NOAA Technical Memorancum NMFS-SEFSC-599. 102 pp. Barros, N.B. 1993. Feeding ecology and foraging strategies of bottlenose dolphins on the central east coast of Florida. Ph.D. Dissertation. University of Miami, Coral Gables, FL. 328 pp. Barros, N.B., and D.K. Odell. 1990. Food habits of the bottlenose dolphins in the Southeastern United States. Pp. 309–328, In S. Leatherwood, and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Barros, N.B., and R.S. Wells. 1998. Prey and feeding patterns of resident Bottlenose Dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Journal of Mammalogy 79(3):1045–1059. Bearden, C.M. 1964. Distribution and abundance of Atlantic Croaker, Micropogon undulatus in South Carolina. Contributions from Bears Bluff Laboratory, Wadmalaw Island, SC. Report No. 40. 23 pp. Berens McCabe, E.J., D.P. Gannon, N.B. Barros, and R.S. Wells. 2010. Prey selection by resident Common Bottlenose Dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Marine Biology 157:931–942. Bernard, H.J., and A.A. Hohn. 1989. Differences in feeding habits between pregnant and lactating Spotted Dolphins (Stenella attenuata). Journal of Mammalogy 70(1):211–215. Caldwell, D.K., and M.C. Caldwell. 1972. The World of the Bottlenosed Dolphin. J.B. Lippincott Co., Philadelphia, PA. 157 pp. 20 Southeastern Naturalist Vol. 11, No. 1 Campana, S.E. 2004. Photographic Atlas of Fish Otoliths of the Northwest Atlantic Ocean. NRC Research Press, Ottawa, ON, Canada. 284 pp. Chao, L.N. 1978. A basis for classifying Western Atlantic Sciaenidae (Teleostei, Perciformes). NOAA Technical Report, NMFS Circular Number 415. 65 pp. Clarke, M.R. (Ed.). 1986. A Handbook for the Identification of Cephalopod Beaks. Oxford University Press, Oxford, UK. 268 pp. Cockcroft, V.G., and G.J.B. Ross. 1990. Food and feeding of the Indian Ocean Bottlenose dolphin off southern Natal, South Africa. Pp. 295–308, In S. Leatherwood and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Corkeron, P.J., M.M. Bryden, and K.E. Hestrom. 1990. Feeding by bottlenose Dolphins in association with trawling operations in Moreton Bay, Australia. Pp. 329–336, In S. Leatherwood and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Dawson, C.E. 1958. A Study of the biology and life history of the Spot, Leiostomus xanthurus Lacepede, with special reference to South Carolina. Contributions from Bears Bluff Laboratories Report No. 28. Wadmalaw Island, SC. Fertl, D.C. 1994. Occurrence, movements, and behavior of Bottlenose Dolphins (Tursiops truncatus) in association with the shrimp fishery in Galveston Bay, Texas. M.Sc. Thesis. Texas A&M University, College Station, TX. Fish, M.P., and W.H. Mowbray. 1970. Sounds of western north Atlantic fishes: A reference file of underwater biological sounds. Johns Hopkins Press, Baltimore, MD. Gannon, D.P. 2003. Behavioral ecology of an acoustically mediated predator-prey system: Bottlenose Dolphins and sciaenid fishes. Ph.D. Dissertation. Duke University, Durham, NC. 244 pp. Gannon, D.P., and C.M. Taylor. 2007. Acoustic behavior of Atlantic Croaker, Micropogonias undulatus (Sciaenidae). Copeia 1997(1):193–204. Gannon, D.P., and D.M. Waples. 2004. Diets of coastal Bottlenose Dolphins from the US mid-Atlantic coast differ by habitat. Marine Mammal Science 20(3):527–545. Gannon, D.P., N.B. Barros, D.P. Nowacek, A.J. Read, D.M. Waples, and R.S. Wells. 2005. Prey detection by Bottlenose Dolphins (Tursiops truncatus): An experimental test of passive listening hypothesis. Animal Behavior 69(3):709–720. Geraci, J.R., and v.J. Lounsbury. 2005. Marine Mammals Ashore: A Field Guide for Strandings, Second Edition. national Aquarium in Baltimore, Baltimore, MD. 371 pp. Gray, G.A., and H.E. Winn. 1961. Representative ecology and sound production of the toadfishes, Opsanus tau. Ecology 42:274–282. Gregory, W.K. 1959. Fish Skulls: A Study of the Evolution of Natural Mechanisms. Eric Lundberg, Laurel, FL. 481 pp. (originally published in 1933, American Philosophical Society, Volume 23, part 2). Gunter, G. 1942. Contributions to the natural history of the Bottlenose Dolphin, Tursiops truncatus (Montague), on the Texas coast, with particular reference to food habits. Journal of Mammalogy 23:267–276. Gunter, G. 1951. Consumption of shrimp by the Bottle-nosed Dolphin. Journal of Mammalogy 32:465–466. Hersh, S.L., and D.A. Duffield. 1990. Distinction between Northwest Atlantic offshore and coastal Bottlenose Dolphins based on hemoglobin and morphometry. Pp. 129– 139, In S. Leatherwood, and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Hoelzel, A.R., C.W. Potter, and P.B. Best. 1998. Genetic differentiation between parapatric nearshore and offshore populations of the Bottlenose Dolphin. Proceedings of the Royal Society of London 265:1177–1183. 2012 S.M. Pate and W.E. McFee 21 Hoffman, R.J. 1991. History, goals, and achievements of the regional marine mammal stranding network. Pp. 7–17, In J.E. Reynolds and D.K. Odell (Eds.). Marine Mammal Strandings in the United States. NOAA Technical Report NMFS 98. Available online at http://www.nmfs.noaa.gov/publications.htm. Accessed 10 April 2009. Jobling, M., and A. Breiby. 1986. The use and abuse of fish otoliths in studies of feeding habits of marine piscivores. Sarsia 71:265–274. Keiser, Jr., R.K. 1976. Species composition, magnitude, and utilization of the incidental catch of the South Carolina shrimp fishery. South Carolina Marine Resource Center, Charleston, SC. Technical Report Number 16. 94 pp. Krebs, C.J. 1999. Ecological Methodology, 2nd Edition. Addison-Wesley Educational Publishers, Inc. , New York, NY. 620 pp. Leatherwood, S. 1975. Some observations of feeding behavior of Bottle-nosed Dolphins (Tursiops truncatus) in the northern Gulf of Mexico and (Tursiops cf T. gilli) off southern California, Baja California, and Nayarit, Mexico. Marine Fisheries Review 37:10–16. MacArthur, R.H., and E.R. Pianka. 1966. On the optimal use of a patchy environment. American Naturalist 100:603–609. Mann, D.A., J. Bowers-Altman, and R.A. Roundtree. 1997. Sounds produced by the Striped Cusk-eel Ophidion marginatum (Ophidiidae) during courtship and spawning. Copeia 1997:610– 612. McDonough, C. J., W.A. Roumillat, and C.A. Wenner. 2003. Fecundity and spawning season of Striped Mullet (Mugil cephalus L.) in South Carolina estuaries. Fishery Bulletin 101:822–834. Mead, J.G., and C.W. Potter. 1990. Natural history of Bottlenose Dolphins along the central Atlantic coast of the United States. Pp. 165–195, In S. Leatherwood, and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Mead, J.G., and C.W. Potter. 1995. Recognizing two populations of the Bottlenose Dolphin (Tursiops truncatus) off the Atlantic coast of North America: Morphological and ecological considerations. IBI Reports 5:31–44. Mohsin, A.K.M. 1981. Comparative account of the otoliths of the weakfishes (Cynoscion) of the Atlantic and Gulf coasts of the United States. Pertanika 4(2):109–111. Odell, D.K. 1975. Status of aspects of the life history of the Bottlenose Dolphin, Tursiops truncatus, in Florida. Journal of Fishery Research Board of Canada 32:1055–1058. Perrin, W.F., and S.B. Reilly. 1984. Reproduction parameters of dolphins and small whales of the family delphinidae. Report of the International Whaling Commission (Special Issue 6):97–133. Pierce, G.J., and P.R. Boyle. 1991. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology Annual Review (London) 29:409–486. Petricig, R.O. 1995. Bottlenose Dolphins (Tursiops truncatus) in Bull Creek, South Carolina. Ph.D. Dissertation. University of Rhode Island, Kingston, RI. 298 pp. Ramcharitar, J., D.P. Gannon, and A.N. Popper. 2006. Review of the bioacoustics of the family Sciaenidae (croakers and drumfishes). Transactions of the American Fisheries Society 135:1409–1431. Read, A.J., and K.T. Murray. 2000. gross evidence of human-induced mortality in small cetaceans. NOAA Technical Memorandum NMFS-OPR-15. 21 pp. Recks, M.A. 2004. An investigation into the use of blubber fatty acid profiles as a means to determine dietary history of Bottlenose Dolphins (Tursiops truncatus) in estuarine and nearshore coastal waters around Charleston, South Carolina. M.Sc. Thesis. The Graduate School of the College of Charleston, Charleston, SC. 141 pp. 22 Southeastern Naturalist Vol. 11, No. 1 Robertson, K.M., and S.J. Chivers. 1997. Prey occurrence in pantropical Spotted Dolphins, Stenella attenuata, from the eastern tropical Pacific. Fishery Bulletin US 95:334–48. Selzer, L.A., G. Early, P.M. Fiorelli, P.M. Payne, and R. Prescott. 1986. Stranded animals as indicators of prey utilization by Harbor Seals, Phoca vitulina concolor, in southern New England. Fishery Bulletin 84(1):217–220. Shane, S.H. 1990.Comparison of Bottlenose Dolphin behavior in Texas and Florida, with a critique of methods for studying dolphin behavior. Pp. 541–558, In S. Leatherwood, and R.R. Reeves (Eds.). The Bottlenose Dolphin. Academic Press, San Diego, CA. 653 pp. Shealy, M.H., Jr., J.V. Miglarese, and E.B. Joseph. 1974. Bottom fishes of South Carolina estuaries: Relative abundance, seasonal distribution, and length-frequency relationships. South Carolina Marine Research Institute, Charleston, SC. Report 6. 189 pp. South Carolina Department of Natural Resources (SCDNR). 2006. State of South Carolina’s Coastal Resources. Available online at http://www.dnr.state.sc.us/marine/. Accessed 10 April 2009. SCDNR SEAMAP. 2000. Results of Trawling Efforts in the Coastal Habitat of the South Atlantic Bight. Available online at http://www.dnr.sc.gov/marine/mrri/SEAMAP/ SMreports.html. Accessed 6 may 2009. Speakman, T., E. Zolman, J. Adams, R.H. Defran, D. Laska, L. Schwacke, J. Craigie, and P.A. Fair. 2006. Temporal and Spatial Aspects of Bottlenose Dolphin Occurrence in Coastal and Estuarine waters near Charleston, South Carolina. NOAA Technical Memorandum NOS NCCOS 37, Silver Springs, MD. Sprague, M.W., and J.J. Luczkovich. 2001. Do Striped Cusk-Eels, Ophidion marginatum, (Ophidiidae) produce the “chatter” sound attributed to Weakfish, Cynoscion regalis (Sciaenidae)? Copeia 2001(3):854–859. Waring G.T., E. Josephson, C.P. Fairfield and K. Maze-Foley (Eds.). 2006. US Atlantic and Gulf of Mexico Marine Mammal Stock Assessments 2005. NOAA Technical Memorandum 194. Wenner, E.L., W.P. Coon III, M.H. Shealy, Jr., and P.A. Sandifer. 1984. Five-year study of seasonal distribution and abundance of fishes and decapod crustaceans in the Cooper River and Charleston Harbor, South Carolina, prior to diversion. NOAA Technical Report NMFS SSRF-782. Young, R.F., and H.D. Phillips. 2002. Primary production required to support Bottlenose Dolphins in a salt marsh creek system. Marine Mammal Science 18(2):358–373. Zolman, E.S. 1996. Residency patterns, relative abundance, and population ecology of Bottlenose Dolphins (Tursiops truncatus) in the Stono River Estuary, Charleston County, South Carolina. M.Sc. Thesis. The Graduate School of the College of Charleston, Charleston, SC. 128 pp. Zolman, E.S. 2002. Residence patterns of Bottlenose Dolphins (Tursiops truncatus) in the Stono River estuary, Charleston County, South Carolina, USA. Marine Mammal Science 18:879–892.