Physical maturity in common bottlenose dolphins (Tursiops truncatus) from Sarasota Bay,Florida

Cetacean physical maturity is defined by growth cessation and complete fusion of epiphyses to vertebral bodies indicated by invisible sutures. Many studies have shown epiphyseal fusion is highly variable among individuals. In-depth examinations into fusion variability are lacking. We analyzed vertebrae of 37 (n = 21 female, n = 16 male) stranded common bottlenose dolphins (Tursiops truncatus) from the well-studied Gulf of Mexico, Sarasota Bay community. For each specimen, vertebrae were examined by vertebral region for degree of fusion anteriorly and posteriorly of each centrum and categorized from unfused to fused in five degrees. An ordinal logistic regression was used to estimate degree of fusion probability for each epiphysis. The model had fixed effects for age, number of offspring, sex, sexual maturity, and a random effect for epiphysis. Results show that age/reproductive status significantly explains an individual's degree of fusion. Adult females with fewer calves had more fusion than those with more reproductive experience across multiple ages. Access to long-term observational and sample data on the dolphins residing in the area served by Mote Marine Laboratory's Stranding Investigations Program offers a unique opportunity to examine the relationship between energetic demands of reproduction (calcium production/reproductive output) versus preconceived definitions of physical maturity (skeletal fusion) more closely.     

Anthropogenic injuries disrupt social associations of common bottlenose dolphins (Tursiops truncatus) in Sarasota Bay,Florida

Social connectivity is important for measuring the fitness of common bottlenose dolphins (Tursiops truncatus). While interactions in fission-fusion societies vary between individuals, studies show that repeated interactions enhance reproduction and foraging success. Injuries that potentially remove an individual from its association network may disrupt these interactions. Using data from the long-term resident dolphin community in Sarasota Bay, Florida, we investigated how anthropogenic injuries affect the dolphins' social associations by examining the differences before and after injury to individuals. We examined group size, strength, eigenvector centrality, clustering coefficient, and number of triangles and analyzed whether the animal's sex, age class, type of injury, or human intervention affected these values. We found that while group size did not change, injured dolphins had fewer preferred associates (HWI > 0.14) and were found in more fluid groups immediately after injury, but started returning to normal association levels after 2 years. This initial decrease in connectivity was not related to the age, sex, type of injury, or intervention. Despite the fluidity in individual associations, the strongest bonds remained stable, those between mothers and calves and those between male alliance partners. These findings provide some of the first information relating injuries and social networks for animals.     

Recreational fishing depredation and associated behaviors involving common bottlenose dolphins (Tursiops truncatus) in Sarasota Bay,Florida

Odontocete depredation involves stealing or damaging bait or prey already captured by fishing gear. The increase in depredation is of concern for small stocks of cetaceans because interactions with fishing gear can lead to serious injury or mortality through entanglement or ingestion. Using long‐term data sets available for the bottlenose dolphin (Tursiops truncatus) community in Sarasota Bay, Florida, we investigated recreational fishing gear interactions by (1) examining temporal patterns in depredation and associated behaviors from 2000 to 2007; (2) quantifying the behavior of dolphins that depredate or engage in associated behaviors; and (3) identifying factors associated with the rise in depredation locally. The number of incidents of dolphins (primarily adult males) interacting with recreational anglers and boaters increased following 2004. Depredation and associated behaviors increased during red tide lags and tourist seasons during times of prey depletion and heightened angler and boater activity. Dolphins with a history of fishing gear interactions shifted away from natural activity patterns and were more likely to be within 50 m of fishing lines. Recreational fishing gear interactions were attributed to a two percent population decline in Sarasota Bay in 2006 and need to be considered along with other cumulative human impacts in the development of conservation measures for dolphins.     

Severe Karenia brevis red tides influence juvenile bottlenose dolphin (Tursiops truncatus) behavior in Sarasota Bay,Florida

Harmful algal blooms (HABs) are natural stressors in the coastal environment that may be increasing in frequency and severity. This study investigates whether severe red tide blooms, caused by Karenia brevis, affect the behavior of resident coastal bottlenose dolphins in Sarasota Bay, Florida through changes to juvenile dolphin activity budgets, ranging patterns, and social associations. Behavioral observations were conducted on free‐ranging juvenile dolphins during the summer months of 2005–2007, and behavior during red tide blooms was compared to periods of background K. brevis abundance. We also utilized dolphin group sighting data from 2004 to 2007 to obtain comparison information from before the most severe recent red tide of 2005 and incorporate social association information from adults in the study area. We found that coastal dolphins displayed a suite of behavioral changes associated with red tide blooms, including significantly altered activity budgets, increased sociality, and expanded ranging behavior. At present, we do not fully understand the mechanism behind these red tide‐associated behavioral effects, but they are most likely linked to underlying changes in resource availability and distribution. These behavioral changes have implications for more widespread population impacts, including increased susceptibility to disease outbreaks, which may contribute to unusual mortality events during HABs.     

Antibiotic-Resistant Organisms Cultured from Atlantic Bottlenose Dolphins (Tursiops truncatus) Inhabiting Estuarine Waters of Charleston, SC and Indian River Lagoon, FL

Bottlenose dolphins (Tursiops truncatus) from estuarine waters of Indian River Lagoon, FL (IRL) and Charleston, SC (CHS) were cultured to screen for microorganism colonization and to assess antibiotic sensitivity. Swabs (n = 909) were collected from the blowhole, gastric fluid, and feces of 171 individual dolphins The most frequently cultured organisms were Plesiomonas shigelloides (n = 161), Aeromonas hydrophila (n = 144), Escherichia coli (n = 85), and Pseudomonas fluorescens (n = 82). In descending frequency, organisms demonstrated resistance to erythromycin, ampicillin, and cephalothin. Human and animal pathogens resistant to antibiotics used in human and veterinary medicine were cultured. Escherichia coli (E. coli) more often was resistant in IRL dolphins. Three cases of methicillin-resistant Staphylococcus aureus (MRSA) were found at CHS. Emergence of antibiotic resistance is not confined to humans. Bottlenose dolphins may serve as sentinels for transfer of resistance from humans and animals or indicate that antibiotics are reaching the marine environment and causing resistance to emerge through selective pressure and genetic adaptation.     

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.     

Lobomycosis in Bottlenose Dolphins (<Emphasis Type="Italic">Tursiops truncatus</Emphasis>) from the Indian River Lagoon,Florida: Estimation of Prevalence,Temporal Trends,and Spatial Distribution

Lobomycosis (lacaziosis) is a chronic fungal disease of the skin that affects only dolphins and humans. Previous studies have shown a high prevalence of lobomycosis in bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon, Florida (IRL). We studied the occurrence and distribution of lobomycosis in the IRL using photo-identification survey data collected between 1996 and 2006. Our objectives were to (1) determine the sensitivity and specificity of photo-identification for diagnosis of lobomycosis in free-ranging dolphins; (2) determine the spatial distribution of lobomycosis in the IRL; and (3) assess temporal patterns of occurrence. Photographs from 704 distinctly marked dolphins were reviewed for skin lesions compatible with lobomycosis. The presumptive diagnosis was validated by comparing the results of photographic analysis with physical examination and histologic examination of lesion biopsies in 102 dolphins captured and released during a health assessment and 3 stranded dolphins. Twelve of 16 confirmed cases were identified previously by photography, a sensitivity of 75%. Among 89 dolphins without disease, all 89 were considered negative, a specificity of 100%. The prevalence of lobomycosis estimated from photographic data was 6.8% (48/704). Spatial distribution was determined by dividing the IRL into six segments based on hydrodynamics and geographic features. The prevalence ranged from <1% in the Mosquito Lagoon to 16.9% in the south Indian River. The incidence of the disease did not increase during the study period, indicating that the disease is endemic, rather than emerging. In summary, photo-identification is a useful tool to monitor the course of individual and population health for this enigmatic disease.     

Using infrared thermography to assess seasonal trends in dorsal fin surface temperatures of free-swimming bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida

The temperature differential (Δ T ) between a body surface and the environment influences an organism's heat balance. In Sarasota Bay, FL, where ambient water temperature ( T _w) ranges annually from 11° to 33°C, Δ T was investigated in a resident community of bottlenose dolphins ( Tursiops truncatus ). Dorsal fin surface temperatures ( T _dfin) were measured on wild, free-swimming dolphins using infrared thermography. Field and laboratory calibration studies were also undertaken to assess the efficacy of this non-invasive technology in the marine environment. The portability of infrared thermography permitted measurements of T _dfin across the entire range of environmental temperatures experienced by animals in this region. Results indicated a positive, linear relationship between T _dfin and T _w ( r ²= 0.978, P < 0.001). On average, T _dfin was 0.9°C warmer than T _w across seasons, despite the 22°C annual range in T _w. Changes in integumentary and vascular insulation likely account for the stability of Δ T _{dfin − w} and the protection of core temperature ( T _core) across seasons. The high thermal conductivity of water may also influence this Δ T . The use of infrared thermography is an effective, non-invasive method of assessing dorsal fin skin surface temperatures (±1°C) across large numbers of wild, free-swimming dolphins throughout their thermally dynamic aquatic environment.     

Blubber morphology in wild bottlenose dolphins (Tursiops truncatus) from the Southeastern United States: influence of geographic location, age class, and reproductive state

This study investigated blubber morphology and correlations of histological measurements with ontogeny, geography, and reproductive state in live, wild bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Surgical skin-blubber biopsies (N=74) were collected from dolphins during capture-release studies conducted in two geographic locations: Charleston, SC (N=38) and Indian River Lagoon, FL (N=36). Histological analysis of blubber revealed stratification into superficial, middle, and deep layers. Adipocytes of the middle blubber were 1.6x larger in Charleston subadults than in Indian River Lagoon subadults (4,590+/-340 compared to 2,833+/-335 microm2 per cell). Charleston subadult dolphins contained higher levels of total blubber lipids than Charleston adult animals (49.3%+/-1.9% compared to 34.2%+/-1.7%), and this difference was manifested in more adipocytes in the middle blubber layer (19.2+/-0.9 compared to 14.9+/-0.5 cells per field). However, dolphins from Indian River Lagoon did not exhibit this pattern, and the adipocyte cell counts of subadults were approximately equal to those of the adults (16.0+/-1.4 compared to 13.4+/-0.8 cells per field). The colder year-round water temperatures in Charleston compared to Indian River Lagoon may explain these differences. Adipocytes in the deep blubber layer were significantly smaller in lactating and simultaneously pregnant and lactating animals compared to pregnant dolphins (840+/-179, 627+/-333, and 2,776+/-586 microm2 per cell, respectively). Total blubber lipid content and adipocyte size in the deep blubber of mothers with calves decreased linearly with calf length. Lactating females may utilize lipids from the deep blubber during periods of increased energetic demands associated with offspring care. This study demonstrates that ontogeny, geography, and reproductive state may influence morphological parameters such as structural fiber densities and adipocyte numbers and sizes, measured in bottlenose dolphin blubber.     

Population structure of island-associated dolphins: Evidence from photo-identification of common bottlenose dolphins (Tursiops truncatus) in the main Hawaiian Islands

Management agencies often use geopolitical boundaries as proxies for biological boundaries. In Hawaiian waters a single stock is recognized of common bottlenose dolphins, Tursiops truncatus , a species that is found both in open water and near-shore among the main Hawaiian Islands. To assess population structure, we photo-identified 336 distinctive individuals from the main Hawaiian Islands, from 2000 to 2006. Their generally shallow-water distribution, and numerous within-year and between-year resightings within island areas suggest that individuals are resident to the islands, rather than part of an offshore population moving through the area. Comparisons of identifications obtained from Kaua'i/Ni'ihau, O'ahu, the "4-island area," and the island of Hawai'i showed no evidence of movements among these island groups, although movements from Kaua'i to Ni'ihau and among the "4-islands" were documented. A Bayesian analysis examining the probability of missing movements among island groups, given our sample sizes for different areas, indicates that interisland movement rates are less than 1% per year with 95% probability. Our results suggest the existence of multiple demographically independent populations of island-associated common bottlenose dolphins around the main Hawaiian islands.     

Bottlenose dolphin (Tursiops truncatus) social structure in the Shannon Estuary,Ireland, is distinguished by age‐ and area‐related associations

Social and network analyses that incorporate information on individuals within a population enhance our knowledge of complex species. In this study, the social structure of wild bottlenose dolphins in the Shannon Estuary, Ireland, was analyzed by examining the dynamics of the whole population and then of individuals classed by sex, age, and area. One hundred and twenty‐one dolphins were identified during 522 sightings between 2012 and 2015. The mean half‐weight association index (HWI) of the population was 0.07 ± 0.02. The highest HWIs for individuals of known sex were for female‐male pairs. Mean within‐class HWI was significantly higher than mean between‐class HWI for both age and area classes. Ordinations and sociograms were used to visualize social networks. Permutation tests revealed nonrandom associations for the population overall and both between and within classes. Temporal analyses showed associations persisting for >1,000 d. The whole population's best fit model was for two levels of casual acquaintances. Movement analyses demonstrated the use of the inner estuary by only 25% of the population revealing a potential community division by area. The difference between mean HWI when socializing (0.09 ± 0.03) compared to foraging (0.06 ± 0.03) was significant. These results highlight the importance of localized research, reflecting the complexity found in bottlenose dolphin societies globally.     

Morphology of the melon and its tendinous connections to the facial muscles in bottlenose dolphins (Tursiops truncatus)

The melon is a lipid‐rich structure located in the forehead of odontocetes that functions to propagate echolocation sounds into the surrounding aquatic environment. To date, the melon's ability to guide and impedance match biosonar sounds to seawater has been attributed to its unique fatty acid composition. However, the melon is also acted upon by complex facial muscles derived from the m. maxillonasolabialis. The goal of this study was to investigate the gross morphology of the melon in bottlenose dolphins (Tursiops truncatus) and to describe how it is tendinously connected to these facial muscles. Standard gross dissection (N = 8 specimens) and serial sectioning (N = 3 specimens) techniques were used to describe the melon and to identify its connections to the surrounding muscles and blubber in three orthogonal body planes. The dolphin forehead was also thin‐sectioned in three body planes (N = 3 specimens), and polarized light was used to reveal the birefringent collagen fibers within and surrounding the melon. This study identified distinct regions of the melon that vary in shape and display locally specific muscle‐tendon morphologies. These regions include the bilaterally symmetric main body and cone and the asymmetric right and left caudal melon. This study is the first to identify that each caudal melon terminates in a lipid cup that envelopes the echolocation sound generators. Facial muscles of the melon have highly organized tendon populations that traverse the melon and insert into either the surrounding blubber, the connective tissue matrix of the nasal plug, or the connective tissue sheath surrounding the sound generators. The facial muscles and tendons also lie within multiple orthogonal body planes, which suggest that the melon is capable of complex shape change. The results of this study suggest that these muscles could function to change the frequency, beam width, and directionality of the emitted sound beam in bottlenose dolphins. The echolocation sound propagation pathway within the dolphin forehead appears to be a tunable system. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay,Florida

Observations of bottlenose dolphins ( Tursiops truncatus ) in Florida Bay, Florida, between 2002 and 2005 revealed the use of three distinct foraging tactics. The goal of this study was to identify ecological correlates with tactic use and describe the impact of foraging specializations on the overall habitat use and distribution patterns of this dolphin population. Foraging tactics showed strong association with contrasting environmental characteristics, primarily depth. Locations of two of these tactic groups were spatially repulsed. Analyses of sighting histories of individual dolphins observed at foraging events determined that dolphins which employed one tactic never employed the other, and vice versa . Although bottlenose dolphins have plastic foraging behaviors, dolphins in Florida Bay appear to specialize in one tactic and subsequently limit their overall distribution patterns to coincide with habitats that facilitate success using that foraging tactic. This study demonstrates how foraging behavior can be an ecological determinant of overall dolphin habitat use patterns and works to create spatial structure within a population due to consistent mapping of tactics onto environmental variation. These foraging specializations potentially impact the social and demographic patterns of this dolphin population. The possible evolutionary mechanisms behind this intraspecific variation, including resource limitation and social learning, are considered.     

Home Ranges of Bottlenose Dolphins (<Emphasis Type="Italic">Tursiops truncatus</Emphasis>) in the Indian River Lagoon,Florida: Environmental Correlates and Implications for Management Strategies

Photo-identification surveys conducted between 2002 and 2005 were used to determine dolphin home ranges and site fidelity within the Indian River Lagoon (IRL), Florida. The IRL was divided into six segments based on hydrodynamics and geographic features for purposes of characterization. Among the 615 dolphins with identifiable dorsal fins, 339 had ≥6 sightings and were used in segment and linear range analyses. The majority (98%) of dolphins were seen in ≤3 consecutive segments (331/339); of these, 44% (144/331) occurred in two segments, and 33% (109/331) in one segment. No dolphins were observed in all six segments. The largest number of dolphins was sighted in segment 1C (North Indian River). However, the highest density of dolphins was found in segment 2 (North-Central Indian River). Re-sighting rates for dolphins with ≥6 sightings ranged from 2.8 to 8.7 times observed. The mean linear home range varied from 22 to 54 km. Distributional analyses indicated that at least three different dolphin communities exist within the IRL: Mosquito Lagoon, and the North and South Indian River. No statistically significant correlations were found between the total number or density per km² of dolphins and surface water area, salinity, or contaminant loads within segments of the lagoon. These results suggest that dolphins do not selectively avoid areas with relatively unfavorable water quality. IRL dolphins should be studied on smaller spatial scales than currently practiced, and potential anthropogenic impacts should be evaluated based on geographic partitioning.     

Hip bone morphometrics of bottlenose dolphins (Tursiops truncatus) from Adriatic Sea: Sex determination and postnatal development

Bones are frequently the only cetacean samples available in the wild and may be useful for determination of sex, physical maturity, body length, and body mass. We analyzed the postnatal morphological development and morphometric characteristics of the cleaned and dried, paired hip bone (os coxae) from 131 bottlenose dolphins, Tursiops truncatus, (61 females, 70 males; total body length 117–322 cm) ranging in age from neonates to 28 yr, salvaged from Croatian waters of the eastern Adriatic Sea. Adult dolphins exhibited sexual dimorphism in their hip bone morphology and morphometrics: fully‐formed hip bones from males were significantly longer, heavier, and more robust than those from females. Moreover, the fully formed hip bone from males featured a prominent bony tuberosity protruding dorsolaterally from the caudal half that was significantly wider and higher than in females. Morphometric measurements were used to generate classification functions for reliable sex determination (97%). In addition, hip bone length in both sexes correlated tightly with total body length, allowing one measurement to be calculated from the other. Only a single ossification developed in all hip bones although soft tissue attachments and comparative review suggests homological equivalence with the tripartite terrestrial mammal hip bone.     

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.     

The buoyancy of the integument of Atlantic bottlenose dolphins (Tursiops truncatus): Effects of growth,reproduction, and nutritional state

In Atlantic bottlenose dolphins (Tursiops truncatus) the thickness and lipid content of blubber (the integument's specialized hypodermis) varies across ontogeny and with reproductive and nutritional state. Because the integument comprises up to 25% of total body mass in this species, ontogenetic changes in its lipid content may influence whole body buoyancy. The density and volume of the integument were measured and its buoyancy calculated across an ontogenetic series of dolphins and in pregnant and emaciated adults (total n= 45). Regional differences between the metabolically labile trunk integument and the structural tailstock integument were also investigated. Mean densities of both trunk and tailstock integument were similar across life history categories (trunk = 1,040.7 ± 14.1 kg/m³; tailstock = 1,077.1 ± 21.2 kg/m³) and were statistically similar to the density of seawater (1,026 kg/m³). The mean buoyant force of integument from the trunk (−1.01 ± 1.74 N) and tailstock (−0.30 ± 0.21 N) did not vary significantly across ontogeny. In contrast, pregnancy and emaciation did influence the integument's buoyancy, which ranged between 9 N and −45 N in these categories. Although neutral during growth, the integument's contribution to whole body buoyancy can be influenced by an individual's reproductive and nutritional status.     

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.     

Use of a serum-based glomerular filtration rate prediction equation to assess renal function by age, sex, fasting, and health status in bottlenose dolphins (Tursiops truncatus)

Glomerular filtration rate (GFR) is a direct measurement of renal function. Although clearance tests using 24‐h urine collection or blood sample series are gold standards for measuring GFR, serum‐based prediction of GFR based upon the Modification of Diet in Renal Disease (MDRD) Study equation is acceptable for routine use in human adults. The purpose of our study was to assess the ability for a modified MDRD Study equation to predict expected changes in GFR in bottlenose dolphins (Tursiops truncatus) using a healthy dolphin population represented by 1,103 routine serum samples collected from 50 dolphins of all age groups, years 1998–2005. Predicted GFR was also calculated from serum collected from a 32‐yr‐old male dolphin with end‐stage renal disease. The dolphin‐adjusted MDRD equation predicted GFR changes in our population that paralleled what has previously been reported in other mammals, including decreasing predicted GFR with age (P < 0.01), higher predicted GFR in dolphins that had recently eaten (P < 0.01), and rapidly decreasing predicted GFR in the animal with end‐stage renal disease. We conclude that a serum‐based GFR prediction equation may be a feasible means of detecting and tracking renal function in bottlenose dolphins.