Foraging habits in a generalist predator: Sex and age influence habitat selection and resource use among bottlenose dolphins (Tursiops truncatus)

This study examines resource use (diet, habitat use, and trophic level) within and among demographic groups (males, females, and juveniles) of bottlenose dolphins (Tursiops truncatus). We analyzed the δ¹³C and δ¹⁵N values of 15 prey species constituting 84% of the species found in stomach contents. We used these data to establish a trophic enrichment factor (TEF) to inform dietary analysis using a Bayesian isotope mixing model. We document a TEF of 0‰ and 2.0‰ for δ¹³C and δ¹⁵N, respectively. The dietary results showed that all demographic groups relied heavily on low trophic level seagrass‐associated prey. Bayesian standard ellipse areas (SEA_b) were calculated to assess diversity in resource use. The SEA_b of females was nearly four times larger than that of males indicating varied resource use, likely a consequence of small home ranges and habitat specialization. Juveniles possessed an intermediate SEA_b, generally feeding at a lower trophic level compared to females, potentially an effect of natal philopatry and immature foraging skills. The small SEA_b of males reflects a high degree of specialization on seagrass associated prey. Patterns in resource use by the demographic groups are likely linked to differences in the relative importance of social and ecological factors.     

Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus)

A number of dolphin species, though highly mobile, show genetic structure among parapatric and sometimes sympatric populations. However, little is known about the temporal patterns of population structure for these species. Here, we apply Bayesian inference and data from ancient DNA to assess the structure and dynamics of bottlenose dolphin (Tursiops truncatus) populations in the coastal waters of the UK. We show that regional population structure in UK waters is consistent with earlier studies suggesting local habitat dependence for this species in the Mediterranean Sea and North Atlantic. One genetically differentiated UK population went extinct at least 100 years ago and has not been replaced. The data indicate that this was a local extinction, and not a case of historical range shift or contraction. One possible interpretation is a declining metapopulation and conservation need for this species in the UK.     

Assessment of increased serum aminotransferases in a managed Atlantic bottlenose dolphin (Tursiops truncatus) population

Nonspecific chronic hepatitis and increased activities of serum aminotransferases have been reported in cetaceans (dolphins, porpoises, and whales). We identified bottlenose dolphins in our current population with episodic increases in serum aminotransferases, specifically alanine aminotransferase (ALT) and aspartate aminotransferase (AST), and we hypothesized that hematologic and serum biochemical changes in these animals may provide clues as to potential causes of liver disease in cetaceans. A retrospective case-control study involving 1,288 blood samples collected during 1998-2006 from 18 dolphins (six cases and 12 age- and sex-matched healthy controls) was conducted to compare eosinophil and platelet counts; and serum proteins, albumin, globulins, bilirubin, gamma glutamyltransferase (GGT), cholesterol, triglycerides, glucose, iron, and erythrocyte sedimentation rates. Bottlenose dolphins with increased ALT and AST activities were more likely to have higher serum globulins, bilirubin, GGT, iron, glucose, triglycerides, and cholesterol levels, greater erythrocyte sedimentation rates, and lower platelet counts compared to healthy controls. Our findings suggest that dolphins with chronic increases in aminotransferases may have a chronic hepatitis involving iron overload with similar etiologies and pathophysiology compared to terrestrial mammals. Areas for future research include predisposing metabolic risk factors; associations between iron overload and a diabetes-like condition; and a potential overlap syndrome involving autoimmune responses that may or may not be associated with viral infection.     

An evaluation of lipid extraction techniques for interpretation of carbon and nitrogen isotope values in bottlenose dolphin (Tursiops truncatus) skin tissue

We studied the effects of two common chemical extraction techniques on bottlenose dolphin (Tursiops truncatus) skin tissues with the intent to develop a mathematical lipid correction for dolphin skin δ¹³C. One method employs a hot solvent mixture (chloroform and methanol) while the other method requires washing the samples with cold solvent followed by water. The water wash method resulted in significant alteration of tissue δ¹⁵N. We found no correlation between change in sample mass and C/N or between change in sample mass and the change in δ¹³C (Δδ¹³C) following lipid extraction. Although Δδ¹³C was positive following lipid extraction (mean = 1.6‰ and 1.2‰, for the two methods), there was no correlation between C/N and Δδ¹³C for either method. Cumulatively, these results prevented us from applying a mathematical lipid normalization. Based on our findings and consideration of previously reported results, we suggest that applying these extraction techniques to dolphin skin with C/N < 4.5 introduces greater uncertainty than is warranted. We recommend against lipid correction for dolphin skins with C/N < 4.5, but stress that the resulting uncertainty in δ¹³C needs to be accounted for when implementing isotope mixing models to assess diet or organic matter sources.     

Thirty year retrospective evaluation of pneumonia in a bottlenose dolphin Tursiops truncatus population

Pneumonia is one of the most common causes of morbidity in bottlenose dolphins Tursiops truncatus. To better understand associations of pneumonia with demographics, microbiology, pathology, and histopathology, a retrospective study on 42 dolphins from the US Navy Marine Mammal Program dolphin population was conducted (1980 to 2010). A total of 21 (50%) of the dolphins evaluated had pneumonia confirmed by histopathology. Bacterial and fungal pneumonia was present in 42.9 and 28.6% of cases (9 and 6 cases), respectively, with Staphylococcus aureus as the most common confirmed pathogen (4 cases, 19%). Other pathogens identified as the cause of pneumonia were Cryptococcus neoformans, Erysipelothrix rhusiopathiae, Histoplasma capsulatum, parainfluenza virus, Proteus species, Pseudomonas aeruginosa, and Streptococcus zooepidemicus. Neither sex nor age was a predictor of pneumonia. While many of the infections involved disseminated disease, lungs were consistently the most severely affected organs. The present study demonstrates the high susceptibility of dolphins to respiratory infections. Areas that warrant further investigation include eosinophilic pneumonia, chronic infections, co-infections, and metabolic or iron-storage diseases. There is a continuing need to improve the early diagnosis and effective treatment of pneumonia in dolphins.     

Struvite calculus in the vagina of a bottlenose dolphin (Tursiops truncatus)

On 27 January 2000, a struvite calculus was observed in the vagina during necropsy of a 138-cm-long female bottlenose dolphin (Tursiops truncatus) collected from the Stono River, South Carolina (USA). Vaginal calculi have been reported in other species of cetaceans but not in bottlenose dolphins. Urinary tract infection might have been an underlying cause of the calculus. While urinary tract inflammation was not detected by light microscopic evaluation of sections of the urinary tract, it is conceivable that sufficient time had lapsed following voiding of the calculus through the urethra for urinary tract infection to have resolved. To further define the prevalence and significance of urolithiasis, prosectors of dead stranded marine mammals are encouraged to closely observe their urinary and genital tracts for calculi and to submit them for quantitative analysis.     

Conflict and reconciliation behavior trends of the bottlenose dolphin (Tursiops truncatus)

Wild bottlenose dolphin (Tursiops truncatus) populations display societal structures characterized by numerous and frequent changes in group composition, complex social relationships, and high levels of cooperation, attributes also observed in human and nonhuman primate cultures. Maintaining social relationships under such elemental conditions can frequently create conflict—and the opportunity for reconciliation—among group members. The conflict and reconciliation behavior patterns of the chimpanzee (Pan troglodytes) have been studied extensively; trends are well‐documented in the wild and in captivity. Apparent cultural similarities have prompted several analogous studies on wild and captive bottlenose dolphins. This research attempted to corroborate previous efforts by analyzing the social behavior of seven captive bottlenose dolphins to determine the effects of sex and age on the frequency of conflict and reconciliation, and to investigate the incidence of consolatory behavior within the group. A total of 3,428 interactions involving focal animals, 414 of which were conflict episodes, were documented during 261 hr of videotaped observations. Although the sample size precluded meaningful statistical evaluation of the influence of sex on conflict and reconciliation, participant age was a significant determinant of conflict frequency. Conversely, age did not impact frequency of reconciliation, which only occurred after 18% of all conflict interactions. Little to no definitive evidence of consolation was apparent within the study group. While results partially support the findings of previous dolphin reconciliation research, extensive behavioral studies of wild populations should be conducted before generating broad comparisons between human terms and nonhuman behavioral interactions. Zoo Biol 29:567–585, 2010. © 2009 Wiley‐Liss, Inc.     

Anaemia, hypothyroidism and immune suppression associated with polychlorinated biphenyl exposure in bottlenose dolphins (Tursiops truncatus)

Polychlorinated biphenyls (PCBs), persistent chemicals widely used for industrial purposes, have been banned in most parts of the world for decades. Owing to their bioaccumulative nature, PCBs are still found in high concentrations in marine mammals, particularly those that occupy upper trophic positions. While PCB-related health effects have been well-documented in some mammals, studies among dolphins and whales are limited. We conducted health evaluations of bottlenose dolphins (Tursiops truncatus) near a site on the Georgia, United States coast heavily contaminated by Aroclor 1268, an uncommon PCB mixture primarily comprised of octa- through deca-chlorobiphenyl congeners. A high proportion (26%) of sampled dolphins suffered anaemia, a finding previously reported from primate laboratory studies using high doses of a more common PCB mixture, Aroclor 1254. In addition, the dolphins showed reduced thyroid hormone levels and total thyroxine, free thyroxine and triiodothyronine negatively correlated with PCB concentration measured in blubber (p = 0.039, < 0.001, 0.009, respectively). Similarly, T-lymphocyte proliferation and indices of innate immunity decreased with blubber PCB concentration, suggesting an increased susceptibility to infectious disease. Other persistent contaminants such as DDT which could potentially confound results were similar in the Georgia dolphins when compared with previously sampled reference sites, and therefore probably did not contribute to the observed correlations. Our results clearly demonstrate that dolphins are vulnerable to PCB-related toxic effects, at least partially mediated through the endocrine system. The severity of the effects suggests that the PCB mixture to which the Georgia dolphins were exposed has substantial toxic potential and further studies are warranted to elucidate mechanisms and potential impacts on other top-level predators, including humans, who regularly consume fish from the same marine waters.     

Occurrence of a unique sialyl tetrasaccharide in colostrum of a bottlenose dolphin (Tursiops truncatus)

Crude oligosaccharides were recovered from bottlenose dolphin (Tursiops truncatus) colostrum after chloroform/methanol extraction of lipids and protein precipitation, and purified using gel filtration, anion exchange chromatography and high performance liquid chromatography (HPLC). Their chemical structures characterized by NMR spectroscopy were as follows: GalNAc(beta1-4)[Neu5Ac(alpha2-3)]Gal(beta1-4)Glc, Neu5Ac(alpha2-3)Gal(beta1-4)Glc, Neu5Ac(alpha2-6)Gal(beta1-4)Glc and Gal(alpha1-4)Gal(beta1-4)Glc. The monosialyltetrasaccharide and neutral trisaccharide have not previously been found as free forms in any natural sources including milk or colostrum, although these structures have been found in the carbohydrate units of glycosphingolipids GM2 and Gb3.     

Harderian gland ultrastructure of the black sea bottlenose dolphin (Tursiops truncatus ponticus)

Examination of the Harderian gland structure of the Black Sea bottlenose dolphin, Tursiops truncatus ponticus, at macroscopic, microscopic, and electron microscopic levels shows significant sexual dimorphism. The epithelial cells of male and female glands are different cell types, capable of producing chemically different products. Secretory cells in both sexes contain secretion granules that produce a secretion consisting mainly of proteins and carbohydrates, but thought to be sex-specific in composition. The female glands also contain lipid secretion granules. It is suggested that in the bottlenose dolphin the Harderian gland functions to produce sexually distinct pheromones and may have other physiological activities, e.g., participating in local immunological or endocrine-related reactions. © 1994 Wiley-Liss, Inc.     

Age structure of strandings and growth of Lahille's bottlenose dolphin (Tursiops truncatus gephyreus)

This study describes the age structure and sex-specific growth patterns of Lahille's bottlenose dolphins (Tursiops truncatus gephyreus), a subspecies endemic to the Southwest Atlantic Ocean (SWAO). The ages of 120 animals collected in southern Brazil between 1976 and 2017 were determined. We found high frequencies of young animals, mostly males, with no sex bias among adults. A temporal change in the age structure of strandings was observed, and we conclude it is a consequence of increased bycatch rates of young dolphins after 2000. The oldest male and female were 27 and 44 years old, respectively, suggesting that females live longer than males in southern Brazil. Growth curve analysis using Gompertz and Laird-Gompertz growth models estimated asymptotic lengths of 316.5 cm for females and 351.6 cm for males, (reached around 13 and 18 years old, respectively), supporting sexual size dimorphism for the subspecies. A second growth pulse was identified for males. Our work highlights the benefit of long-term studies and contributes valuable information toward understanding the life history of Lahille's bottlenose dolphin. It will serve as baseline for future studies that seek to understand mortality patterns of bottlenose dolphins elsewhere and the effects of anthropogenic actions on the survival of these animals.     

Dietary variations within a family of ambush predators (Platycephalidae) occupying different habitats and environments in the same geographical region

This study has determined the extents and basis for variations in the composition of the prey ingested by the abundant species of a family highly adapted for ambush predation, i.e. Platycephalidae, in a region (south‐western Australia) where that family is found in different habitats and environments. Dietary data were thus collected for Leviprora inops and Platycephalus laevigatus from seagrass in marine embayments and for Platycephalus westraliae from over sand in an estuary. These were then collated with those recorded previously for Platycephalus speculator from over sand and in seagrass in an estuary and for Platycephalus longispinis from over sand in coastal marine waters. While crustaceans and teleosts together dominated the diet of all five species, their percentage volumetric dietary contributions varied greatly, with those of crustaceans ranging from 7% for L. inops to 65% for P. speculator and those of teleosts ranging from 29% for P. longispinis to 91% for L. inops. For analyses, the data were separated into two sets. The first comprised the 17 dietary categories of invertebrates and all identified and unidentified teleosts collectively, while the second consisted of the 23 identified teleost families, both of which were subjected to permutational analysis of variance (PERMANOVA), analysis of similarities (ANOSIM) and a new (two‐way) version of the RELATE procedure. The diets of three species changed seasonally, when using invertebrate dietary categories and teleosts collectively, but with only one species, when employing identified teleost families, probably reflecting a greater tendency for invertebrate than teleost prey abundance to change during the year. On the basis of dietary data for invertebrate taxa + teleosts collectively, the diets of three of the five species changed serially with body size, with a fourth species feeding, throughout life, predominantly on the carid Palaemonetes australis. Based on identified teleost families, the diets of the three species that fed predominantly on teleosts underwent serial size‐related changes. Although L. inops and the co‐occurring P. laevigatus both consume large volumes of teleosts, the former ingests larger, less demersal and more mobile prey, e.g. the labrids Haletta semifasciata and Neoodax balteatus, than the latter, e.g. the scorpaenid Gymnapistes marmoratus, reflecting the possession by L. inops of a far longer head and larger buccal cavity. Circumstantial evidence suggests that the large differences in the volumes of crustaceans and teleosts consumed by each platycephalid species are related to differences in the relative availability of these prey in the different habitats or environments of each species.     

Effect of cryopreservation methods and precryopreservation storage on bottlenose dolphin (Tursiops truncatus) spermatozoa

Research was conducted to develop an effective method for cryopreserving bottlenose dolphin (Tursiops truncatus) semen processed immediately after collection or after 24-h liquid storage. In each of two experiments, four ejaculates were collected from three males. In experiment 1, three cryopreservation methods (CM1, CM2, and CM3), two straw sizes (0.25 and 0.5 ml), and three thawing rates (slow, medium, and fast) were evaluated. Evaluations were conducted at collection, prefreeze, and 0-, 3-, and 6-h postthaw. A sperm motility index (SMI; total motility [TM] x % progressive motility [PPM] x kinetic rating [KR, scale of 0-5]) was calculated and expressed as a percentage MI of the initial ejaculate. For all ejaculates, initial TM and PPM were greater than 85%, and KR was five. At 0-h postthaw, differences in SMI among cryopreservation methods and thaw rates were observed (P < 0.05), but no effect of straw size was observed. In experiment 2, ejaculates were divided into four aliquots for dilution (1:1) and storage at 4 degrees C with a skim milk- glucose or a N-tris(hydroxymethyl)methyl-2-aminoethane sulfonic acid (TES)-TRIS egg yolk solution and at 21 degrees C with a Hepes-Tyrode balanced salt solution (containing bovine albumin and HEPES) (TALP) medium or no dilution. After 24 h, samples were frozen and thawed (CM3, 0.5-ml straws, fast thawing rate) at 20 x 10(6) spermatozoa ml(-1) (low concentration) or at 100 x 10(6) spermatozoa ml(-1) (standard concentration). The SMI at 0-h postthaw was higher for samples stored at 4 degrees C than for samples stored at 21 degrees C (P < 0.001), and at 6-h postthaw, the SMI was higher for samples frozen at the standard concentration than for samples frozen at the low concentration (P < 0.05). For both experiments, acrosome integrity was similar across treatments. In summary, a semen cryopreservation protocol applied to fresh or liquid-stored semen maintained high levels of initial ejaculate sperm characteristics.     

Decline in local abundance of bottlenose dolphins (Tursiops truncatus) in the Bay of Islands,New Zealand

Regional populations of bottlenose dolphins (Tursiops truncatus) around New Zealand are genetically isolated from each other and the species was recently classified as nationally endangered based on relatively small population sizes and reports of high calf mortality. Here, we estimate the abundance and trends in one of these regional populations, the Bay of Islands, using a photo‐identification database collected from 1997 to 1999 and from 2003 to 2006, containing a total of 3,841 records of 317 individual dolphins. Estimates of abundance obtained with the robust design fluctuated widely but showed a significant decline in the number of dolphins present in the bay over time (7.5% annual rate of decline). Temporary emigration was random and fluctuated considerably (γ  =  0.18, SE = 0.07 to γ  =  0.84, SE = 0.06). Apparent survival was estimated at 0.928 (CI = 0.911–0.942). Seasonal estimates (26 seasons) obtained in POPAN also showed a significant decline in abundance (5.8% annual rate of decline). Despite the decline observed in local abundance, dolphins continue to be found regularly in the Bay of Islands, suggesting that fewer dolphins use the bay on regular basis. Consequently, it seems that a change in habitat use, mortality and possibly low recruitment could underlie the apparent local decline.     

Molecular cloning and histological localization of LH-like substances in a bottlenose dolphin (Tursiops truncatus) placenta

All mammals exhibit pituitary-specific expression of LH and FSH, whereas placental expression of gonadotropins has been reported only in primates and equids. Some cetaceans, such as dolphins, have a long gestational period and a sexual cycle of about 27 days almost comparable with that of humans. Histologically, dolphins have an epitheliochorial placentae that resembles placentas of Perissodactyla including horses. In the present study, we cloned cDNAs encoding gonadotropins and observed their immunohistochemical localization in the placenta of bottlenose dolphin. The cDNAs obtained encoded 120 amino acids for the alpha-subunit (including 96 amino acids of mature proteins), and 141 amino acids for the beta-subunit (including 121 amino acids of mature proteins). The sequence of the alpha-subunit was similar to that in the pig (Artiodactyla) pituitary glycoprotein hormone [96.7% homology at amino acids (aa) level], and the sequence of the beta-subunit was similar to that of luteinizing hormone (LH) in the pig [94.3% homology at aa level] and white rhinoceros (Perissodactyla) [93.3% homology at aa level]. Of interest, dolphin LHbeta lacks carboxyl-terminal-peptides (CTP). This fact suggests that CTP are not essential for placental expression of gonadotropin in dolphins. Immunohistochemical observations employing anti-ovine LHbeta antibody revealed positive staining in the villositycal tissue. Our observations suggest placental expression of gonadotropin homologues in cetaceans and possible evolutionary conservation of placentae-derived hormonal control of ovarian functions during pregnancy.     

First report of Streptococcus agalactiae and Lactococcus garvieae from a wild bottlenose dolphin (Tursiops truncatus)

The isolation and characterization of two bacterial species, Streptococcus agalactiae and Lactococcus garvieae, previously unreported in wild marine mammals are described from a freshly dead bottlenose dolphin, Tursiops truncatus, from Kuwait Bay, Kuwait, in September 2001. Conventional and rapid identification systems were used to determine that isolates from muscle and kidney were S. agalactiae and L. garvieae, respectively. The isolates were gram-positive, catalase-negative, oxidase-negative, nonhemolytic cocci. The S. agalactiae was serotyped to group antigen B, whereas the L. garvieae could not be assigned to any serogroup. These Kuwait isolates displayed considerable homogeneity with corresponding American Type Culture Collection (ATCC) type isolates. Although the dolphin S. agalactiae isolate was nonhemolytic, it was biochemically similar to S. agalactiae isolated from mullet sampled in the concurrent Kuwait Bay fish kill. Some biochemical heterogeneity was observed between the dolphin isolates and corresponding mammalian ATCC type isolates, especially with Voges Proskauer, alanine-phenylanaline-proline arylamidase, and alpha-galactosidase tests. Nile tilapia, Oreochromis niloticus, experimentally infected with the dolphin S. agalactiae and L. garvieae isolates experienced 90% and 0% mortalities, respectively. This is the first isolation of S. agalactiae and L. garvieae from a wild marine mammal, and the microbial characteristics established here provide pertinent information for the future isolation of these bacteria.     

Retrospective analysis of bottlenose dolphin foraging: A legacy of anthropogenic ecosystem disturbance

We used stable isotope analysis to investigate the foraging ecology of coastal bottlenose dolphins (Tursiops truncatus) in relation to a series of anthropogenic disturbances. We first demonstrated that stable isotopes are a faithful indicator of habitat use by comparing muscle isotope values to behavioral foraging data from the same individuals. δ¹³C values increased, while δ³⁴S and δ¹⁵N values decreased with the percentage of feeding observations in seagrass habitat. We then utilized stable isotope values of muscle to assess temporal variation in foraging habitat from 1991 to 2010 and collagen from tooth crown tips to assess the time period 1944 to 2007. From 1991 to 2010, δ¹³C values of muscle decreased while δ³⁴S values increased indicating reduced utilization of seagrass habitat. From 1944 to 1989 δ¹³C values of the crown tip declined significantly, likely due to a reduction in the coverage of seagrass habitat and δ¹⁵N values significantly increased, a trend we attribute to nutrient loading from a rapidly increasing human population. Our results demonstrate the utility of using marine mammal foraging habits to retrospectively assess the extent to which anthropogenic disturbance impacts coastal food webs.     

Histologic findings in free-ranging Sarasota Bay bottlenose dolphin (Tursiops truncatus) skin: mercury, selenium, and seasonal factors

Full-thickness epidermal biopsy samples were collected from free-ranging common bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida, USA. Season (summer or winter) of collection, mercury (Hg) concentration, and selenium (Se) concentration were compared to histologic parameters. Epidermal Hg concentration was positively related to age (P<0.001) and negatively related to height of the stratum spinosum (P<0.05). The mitotic index and heights of the stratum externum and intermedium were lower in summer than in winter (P<0.01). Transmission electron microscopic examination revealed variation in the diameters (60-138 nm) and arrangements of collagen fibers, regardless of age or concentrations of Hg and Se. The significance of the variation in height of the stratum spinosum and the perivascular collagen degeneration to dolphin health need further investigation.