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1.  Pathology of morbillivirus infection in striped dolphins (Stenella coeruleoalba) from Valencia and Murcia, Spain. 
During the summer and fall of 1990 hundreds of striped dolphins (Stenella coeruleoalba) died in the Spanish Mediterranean as a result of morbillivirus infection. A pathological investigation was carried out on dolphins from Valencia and Murcia which were among the first to die in the epizootic. The dolphins were in poor body condition and pneumonia was the main necropsy finding. Microscopic lung lesions characterized by necrosis of bronchial and bronchiolar epithelium and infiltration of alveoli with macrophages, lymphocytes, neutrophils and multinucleated syncytia were seen in most dolphins. Cytoplasmic and nuclear eosinophilic viral inclusions were present in bronchial and bronchiolar epithelium and in syncytia. Focal granulomatous inflammation associated with nematodes was also present. Brain lesions included diffuse degeneration and necrosis of neurons, microgliosis, perivascular cuffing, formation of syncytia and focal demyelination. Cytoplasmic and nuclear eosinophilic inclusions were present in neurons and glial cells. There was severe lymphoid necrosis and depletion of spleen and lymph nodes and syncytia also occurred in lymph nodes. Biliary and transitional epithelium contained nuclear and cytoplasmic eosinophilic inclusions. Immunoperoxidase staining using monoclonal antibodies to phocine distemper virus confirmed the presence of morbillivirus antigens in lung and brain. The distribution and severity of lesions in striped dolphins are similar to those of distemper in seals, harbor porpoises and terrestrial mammals. The formation of syncytia in the lung and brain may be a useful pathological indicator of morbillivirus infection and may be used in the investigation of pinniped and cetacean strandings in North America.
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PMCID: PMC1263546  PMID: 1423061
2.  Monoclonal Antibody-Based Competitive Enzyme-Linked Immunosorbent Assay for Detection of Morbillivirus Antibody in Marine Mammal Sera 
Journal of Clinical Microbiology  2001;39(5):1877-1881.
A competitive enzyme-linked immunosorbent assay (cELISA), using two monoclonal antibodies (MAbs), was developed and compared with the standard virus neutralization test (VNT) for detecting antibodies against canine distemper virus (CDV) and phocine distemper virus (PDV) in sera from dogs and various species of marine mammals. The test depends on the blocking of MAb binding to solid-phase antigen in the presence of positive serum. Test conditions were optimized by using control VNT-negative and -positive sera specific for CDV and PDV. A positive cutoff value of 30% inhibition, which represents the mean cutoff of a VNT-negative population (n = 623) plus 2 standard deviations, was adopted for the test. A total of 736 serum samples were tested by the new cELISA and by the VNT as the “gold standard.” An unexpected but useful finding was the ability of this CDV- and PDV-specific cELISA to also detect antibodies against the related pair dolphin morbillivirus and porpoise morbillivirus. Based on a subpopulation of 625 sera used in statistical analyses, the overall sensitivity and specificity of cELISA relative to those of the VNT were 94.9 and 97.7%, respectively. Because the cELISA proved to be nearly as sensitive and specific as the VNT while being simpler and more rapid, it would be an adequate screening test for suspect CDV or PDV cases and would also be useful for epidemiological surveillance of morbilliviral infections in marine mammal populations.
doi:10.1128/JCM.39.5.1877-1881.2001
PMCID: PMC88042  PMID: 11326007
3.  Patterns of Dolphin Bycatch in a North-Western Australian Trawl Fishery 
PLoS ONE  2014;9(4):e93178.
The bycatch of small cetaceans in commercial fisheries is a global wildlife management problem. We used data from skippers' logbooks and independent observers to assess common bottlenose dolphin (Tursiops truncatus) bycatch patterns between 2003 and 2009 in the Pilbara Trawl Fishery, Western Australia. Both datasets indicated that dolphins were caught in all fishery areas, across all depths and throughout the year. Over the entire datasets, observer reported bycatch rates (n = 52 dolphins in 4,124 trawls, or 12.6 dolphins/1,000 trawls) were ca. double those reported by skippers (n = 180 dolphins in 27,904 trawls, or 6.5 dolphins/1,000 trawls). Generalised Linear Models based on observer data, which better explained the variation in dolphin bycatch, indicated that the most significant predictors of dolphin catch were: (1) vessel - one trawl vessel caught significantly more dolphins than three others assessed; (2) time of day – the lowest dolphin bycatch rates were between 00:00 and 05:59; and (3) whether nets included bycatch reduction devices (BRDs) - the rate was reduced by ca. 45%, from 18.8 to 10.3 dolphins/1,000 trawls, after their introduction. These results indicated that differences among vessels (or skippers' trawling techniques) and dolphin behavior (a diurnal pattern) influenced the rates of dolphin capture; and that spatial or seasonal adjustments to trawling effort would be unlikely to significantly reduce dolphin bycatch. Recent skipper's logbook data show that dolphin bycatch rates have not declined since those reported in 2006, when BRDs were introduced across the fishery. Modified BRDs, with top-opening escape hatches from which dolphins might escape to the surface, may be a more effective means of further reducing dolphin bycatch. The vulnerability of this dolphin population to trawling-related mortality cannot be assessed in the absence of an ongoing observer program and without information on trawler-associated dolphin community size, broader dolphin population size and connectivity with adjacent populations.
doi:10.1371/journal.pone.0093178
PMCID: PMC3973695  PMID: 24695338
4.  Morbillivirus Downregulation of CD46 
Journal of Virology  1998;72(12):10292-10297.
There is evidence that CD46 (membrane cofactor protein) is a cellular receptor for vaccine and laboratory-passaged strains of measles virus (MV). Following infection with these MV strains, CD46 is downregulated from the cell surface, and consequent complement-mediated lysis has been shown to occur upon infection of a human monocytic cell line. The MV hemagglutinin (H) protein alone is capable of inducing this downregulation. Some wild-type strains of MV fail to downregulate CD46, despite infection being prevented by anti-CD46 antibodies. In this study we show that CD46 is also downregulated to the same extent by wild-type, vaccine, and laboratory-passaged strains of rinderpest virus (RPV), although CD46 did not appear to be the receptor for RPV. Expression of the RPV H protein by a nonreplicating adenovirus vector was also found to cause this downregulation. A vaccine strain of peste des petits ruminants virus caused slight downregulation of CD46 in infected Vero cells, while wild-type and vaccine strains of canine distemper virus and a wild-type strain of dolphin morbillivirus failed to downregulate CD46. Downregulation of CD46 can, therefore, be a function independent of the use of this protein as a virus receptor.
PMCID: PMC110616  PMID: 9811778
5.  Platelet-Rich Plasma and Adipose-Derived Mesenchymal Stem Cells for Regenerative Medicine-Associated Treatments in Bottlenose Dolphins (Tursiops truncatus) 
PLoS ONE  2014;9(9):e108439.
Dolphins exhibit an extraordinary capacity to heal deep soft tissue injuries. Nevertheless, accelerated wound healing in wild or captive dolphins would minimize infection and other side effects associated with open wounds in marine animals. Here, we propose the use of a biological-based therapy for wound healing in dolphins by the application of platelet-rich plasma (PRP). Blood samples were collected from 9 different dolphins and a specific and simple protocol which concentrates platelets greater than two times that of whole blood was developed. As opposed to a commonly employed human protocol for PRP preparation, a single centrifugation for 3 minutes at 900 rpm resulted in the best condition for the concentration of dolphin platelets. By FACS analysis, dolphin platelets showed reactivity to platelet cell-surface marker CD41. Analysis by electron microscopy revealed that dolphin platelets were larger in size than human platelets. These findings may explain the need to reduce the duration and speed of centrifugation of whole blood from dolphins to obtain a 2-fold increase and maintain proper morphology of the platelets. For the first time, levels of several growth factors from activated dolphin platelets were quantified. Compared to humans, concentrations of PDGF-BB were not different, while TGFβ and VEGF-A were significantly lower in dolphins. Additionally, adipose tissue was obtained from cadaveric dolphins found along the Spanish Mediterranean coast, and adipose-derived mesenchymal stem cells (ASCs) were successfully isolated, amplified, and characterized. When dolphin ASCs were treated with 2.5 or 5% dolphin PRP they exhibited significant increased proliferation and improved phagocytotic activity, indicating that in culture, PRP may improve the regenerative capacity of ASCs. Taken together, we show an effective and well-defined protocol for efficient PRP isolation. This protocol alone or in combination with ASCs, may constitute the basis of a biological treatment for wound-healing and tissue regeneration in dolphins.
doi:10.1371/journal.pone.0108439
PMCID: PMC4177220  PMID: 25251412
6.  Development and Application of Specific Cytokine Assays in Tissue Samples from a Bottlenose Dolphin with Hyperinsulinemia 
Chronic inflammation has been associated with insulin resistance and type 2 diabetes (T2D) in humans. Postmortem hepatic and splenic tissue from a 46-year-old geriatric male bottlenose dolphin (Tursiops truncatus) with insulin resistance (chronic hyperinsulinemia with hyperglycemia), chronic inflammation (white blood cell count greater than 12,000 cells/μL), and mild fatty liver disease was evaluated for elevated pro-inflammatory mediators. Cytokine mRNA expression in postmortem hepatic and splenic tissue, as determined by real-time PCR, included an array of cytokines: TGF-β, TNF-α, IFN-γ, IL-2, IL-4, IL-10, IL-12p40, IL-13, and IL-18. Values from this dolphin were compared to a younger reference dolphin with no known chronic metabolic perturbations or inflammation. Levels of TGF-β, TNF-α, and IL-4 were higher in the case dolphin’s liver compared to that of the reference dolphin. In the case dolphin’s spleen, IL-10 and IFN-γ mRNA was upregulated while IL-4 was less than the reference dolphin. IL-18 and IL-13 were upregulated in both tissues. Fluorescent immunohistochemistry (IHC) utilized the following antibodies: anti-porcine IL-6, anti-bovine IFN-γ, IL-4, and IL-10, anti-human TGF-β, anti-ovine IL-1β, and anti-dolphin IL-8. Fluorescent IHC in spleen from the case dolphin revealed staining of IL-4, IL-6, IL-8, and TGF-β throughout the tissue. IL-10 and IFN-γ were seen to predominate in areas surrounding the follicles of splenic tissue. This is the first characterization of cytokine levels in dolphin hepatic and splenic tissue. While there are limitations to a case study, this report of inflammatory biomarkers in tissues of a dolphin with insulin resistance and fatty liver disease are similar to those observed in human patients.
doi:10.3389/fendo.2013.00134
PMCID: PMC3787309  PMID: 24101915
Tursiops truncatus; hyperinsulinemia; diabetes; inflammation; cytokines; real-time PCR; immunohistochemistry
7.  Evaluation of Potential Protective Factors Against Metabolic Syndrome in Bottlenose Dolphins: Feeding and Activity Patterns of Dolphins in Sarasota Bay, Florida 
Free-ranging bottlenose dolphins (Tursiops truncatus) living in Sarasota Bay, Florida appear to have a lower risk of developing insulin resistance and metabolic syndrome compared to a group of dolphins managed under human care. Similar to humans, differences in diet and activity cycles between these groups may explain why Sarasota dolphins have lower insulin, glucose, and lipids. To identify potential protective factors against metabolic syndrome, existing and new data were incorporated to describe feeding and activity patterns of the Sarasota Bay wild dolphin community. Sarasota dolphins eat a wide variety of live fish and spend 10–20% of daylight hours foraging and feeding. Feeding occurs throughout the day, with the dolphins eating small proportions of their total daily intake in brief bouts. The natural pattern of wild dolphins is to feed as necessary and possible at any time of the day or night. Wild dolphins rarely eat dead fish or consume large amounts of prey in concentrated time periods. Wild dolphins are active throughout the day and night; they may engage in bouts of each key activity category at any time during daytime. Dive patterns of radio-tagged dolphins varied only slightly with time of day. Travel rates may be slightly lower at night, suggesting a diurnal rhythm, albeit not one involving complete, extended rest. In comparison, the managed dolphins are older; often fed a smaller variety of frozen-thawed fish types; fed fish species not in their natural diet; feedings and engaged activities are often during the day; and they are fed larger but fewer meals. In summary, potential protective factors against metabolic syndrome in dolphins may include young age, activity, and small meals fed throughout the day and night, and specific fish nutrients. These protective factors against insulin resistance and type 2 diabetes are similar to those reported in humans. Further studies may benefit humans and dolphins.
doi:10.3389/fendo.2013.00139
PMCID: PMC3794307  PMID: 24133483
metabolic disease; diet; age; bottlenose dolphin; activity cycles; foraging; telemetry
8.  Dolphins Can Maintain Vigilant Behavior through Echolocation for 15 Days without Interruption or Cognitive Impairment 
PLoS ONE  2012;7(10):e47478.
In dolphins, natural selection has developed unihemispheric sleep where alternating hemispheres of their brain stay awake. This allows dolphins to maintain consciousness in response to respiratory demands of the ocean. Unihemispheric sleep may also allow dolphins to maintain vigilant states over long periods of time. Because of the relatively poor visibility in the ocean, dolphins use echolocation to interrogate their environment. During echolocation, dolphin produce clicks and listen to returning echoes to determine the location and identity of objects. The extent to which individual dolphins are able to maintain continuous vigilance through this active sense is unknown. Here we show that dolphins may continuously echolocate and accurately report the presence of targets for at least 15 days without interruption. During a total of three sessions, each lasting five days, two dolphins maintained echolocation behaviors while successfully detecting and reporting targets. Overall performance was between 75 to 86% correct for one dolphin and 97 to 99% correct for a second dolphin. Both animals demonstrated diel patterns in echolocation behavior. A 15-day testing session with one dolphin resulted in near perfect performance with no significant decrement over time. Our results demonstrate that dolphins can continuously monitor their environment and maintain long-term vigilant behavior through echolocation.
doi:10.1371/journal.pone.0047478
PMCID: PMC3474785  PMID: 23082170
9.  Comparison of Temporal Parameters of Swimming Rescue Elements When Performed Using Dolphin and Flutter Kick with Fins - Didactical Approach 
The aim of this study was an analysis of the time required to swim to a victim and tow them back to shore, while perfoming the flutter-kick and the dolphin-kick using fins. It has been hypothesized that using fins while using the dolphin-kick when swimming leads to reduced rescue time. Sixteen lifeguards took part in the study. The main tasks performed by them, were to approach and tow (double armpit) a dummy a distance of 50m while applying either the flutter-kick, or the dolphin-kick with fins. The analysis of the temporal parameters of both techniques of kicking demonstrates that, during the approach to the victim, neither the dolphin (tmean = 32.9s) or the flutter kick (tmean = 33.0s) were significantly faster than the other. However, when used for towing a victim the flutter kick (tmean = 47.1s) was significantly faster when compared to the dolphin-kick (tmean = 52.8s). An assessment of the level of technical skills in competitive swimming, and in approaching and towing the victim, were also conducted. Towing time was significantly correlated with the parameter that linked the temporal and technical dimensions of towing and swimming (difference between flutter kick towing time and dolphin-kick towing time, 100m medley time and the four swimming strokes evaluation). No similar interdependency has been discovered in flutter kick towing time. These findings suggest that the dolphin-kick is a more difficult skill to perform when towing the victim than the flutter-kick. Since the hypothesis stated was not confirmed, postulates were formulated on how to improve dolphin-kick technique with fins, in order to reduce swimming rescue time.
Key points
The source of reduction of swimming rescue time was researched.
Time required to approach and to tow the victim while doing the flutter kick and the dolphin-kick with fins was analyzed.
The propulsion generated by dolphin-kick did not make the approach and tow faster than the flutter kick.
More difficult skill to realize of dolphin-kick than the flutter-kick was postulated.
The criteria for how improve dolphin kick technique with fins were formulated.
PMCID: PMC3763315  PMID: 24150079
Swimming; lifesaving; dolphin kick; fins; rescue tow
10.  Comparison of Nephrolithiasis Prevalence in Two Bottlenose Dolphin (Tursiops truncatus) Populations 
In humans, ammonium urate (AU) nephrolithiasis is rare in the Western hemisphere and more common in Japan and developing countries. Among a variety of risk factors, insulin resistance has been associated with urate nephrolithiasis in people. Bottlenose dolphins (Tursiops truncatus) are susceptible to AU nephrolithiasis, and it is believed that some populations are more likely to develop nephrolithiasis compared to others. In an effort to better understand population-based risk factors for AU nephrolithiasis in dolphins and their comparative value to humans, sonographic evaluation was performed on dolphins from a managed collection in San Diego Bay, CA (n = 40) and dolphins from a free-ranging, nearshore population in Sarasota Bay, FL (n = 39) to look for evidence of nephrolithiasis. While 14 (35%) of San Diego Bay dolphins evaluated for the study had sonographic evidence of nephrolithiasis, none of the Sarasota Bay dolphins had evidence of disease. Presence or absence of stones was confirmed by computed tomography in a subset of the San Diego collection (n = 10; four dolphins with stones, six without stones). Age was identified as a risk factor, as dolphins with stones in the San Diego collection were significantly older than dolphins without stones (25.4 vs. 19.1 years, respectively; P = 0.04). Additionally, San Diego dolphins included in the study were significantly older than Sarasota Bay dolphins (21.3 vs. 13.8 years, respectively; P = 0.008). In addition to the previously reported risk factors of hypocitraturia and hyperinsulinemia in bottlenose dolphins, other potential factors include geographic location, managed vs. free-ranging status, prey species, and feeding schedules.
doi:10.3389/fendo.2013.00145
PMCID: PMC3797464  PMID: 24137158
urate nephrolithiasis; dolphins; Tursiops truncatus; ultrasound; computed tomography; age
11.  Common Dolphin (Delphinus delphis) Bycatch in New Zealand Commercial Trawl Fisheries 
PLoS ONE  2013;8(5):e64438.
Marine mammals are regularly reported as bycatch in commercial and artisanal fisheries, but data are often insufficient to allow assessment of these incidental mortalities. Observer coverage of the mackerel trawl fishery in New Zealand waters between 1995 and 2011 allowed evaluation of common dolphin Delphinus delphis bycatch on the North Island west coast, where this species is the most frequently caught cetacean. Observer data were used to develop a statistical model to estimate total captures and explore covariates related to captures. A two-stage Bayesian hurdle model was used, with a logistic generalised linear model predicting whether any common dolphin captures occurred on a given tow of the net, and a zero-truncated Poisson distribution to estimate the number of dolphin captures, given that there was a capture event. Over the 16-year study period, there were 119 common dolphin captures reported on 4299 observed tows. Capture events frequently involved more than one individual, with a maximum of nine common dolphin observed caught in a single tow. There was a peak of 141 estimated common dolphin captures (95% c.i.: 56 to 276; 6.27 captures per 100 tows) in 2002–03, following the marked expansion in annual effort in this fishery to over 2000 tows. Subsequently, the number of captures fluctuated although fishing effort remained relatively high. Of the observed capture events, 60% were during trawls where the top of the net (headline) was <40 m below the surface, and the model determined that this covariate best explained common dolphin captures. Increasing headline depth by 21 m would halve the probability of a dolphin capture event on a tow. While lack of abundance data prevents assessment of the impact of these mortalities on the local common dolphin population, a clear recommendation from this study is the increasing of headline depth to reduce common dolphin captures.
doi:10.1371/journal.pone.0064438
PMCID: PMC3661492  PMID: 23717614
12.  Blood-Based Indicators of Insulin Resistance and Metabolic Syndrome in Bottlenose Dolphins (Tursiops truncatus) 
Similar to people with metabolic syndrome, bottlenose dolphins (Tursiops truncatus) can have a sustained postprandial hyperglycemia and hyperinsulinemia, dyslipidemia, and fatty liver disease. A panel of potential postprandial blood-based indicators of insulin resistance and metabolic syndrome were compared among 34 managed collection dolphins in San Diego Bay, CA, USA (Group A) and 16 wild, free-ranging dolphins in Sarasota Bay, FL, USA (Group B). Compared to Group B, Group A had higher insulin (2.1 ± 2.5 and 13 ± 13 μIU/ml), glucose (87 ± 19 and 108 ± 12 mg/dl), and triglycerides (75 ± 28 and 128 ± 45 mg/dl) as well as higher cholesterol (total, high-density lipoprotein cholesterol, and very low density lipoprotein cholesterol), iron, transferrin saturation, gamma-glutamyl transpeptidase (GGT), alanine transaminase, and uric acid. Group A had higher percent unmodified adiponectin. While Group A dolphins were older, the same blood-based differences remained when controlling for age. There were no differences in body mass index (BMI) between the groups, and comparisons between Group B and Group A dolphins have consistently demonstrated lower stress hormones levels in Group A. Group A dolphins with high insulin (greater than 14 μIU/ml) had higher glucose, iron, GGT, and BMI compared to Group A dolphins with lower insulin. These findings support that some dolphin groups may be more susceptible to insulin resistance compared to others, and primary risk factors are not likely age, BMI, or stress. Lower high-molecular weight adiponectin has been identified as an independent risk factor for type 2 diabetes in humans and may be a target for preventing insulin resistance in dolphins. Future investigations with these two dolphin populations, including dietary and feeding differences, may provide valuable insight for preventing and treating insulin resistance in humans.
doi:10.3389/fendo.2013.00136
PMCID: PMC3793200  PMID: 24130551
adiponectin; bottlenose dolphin; diabetes; insulin resistance; iron; metabolic syndrome
13.  Population Differentiation and Hybridisation of Australian Snubfin (Orcaella heinsohni) and Indo-Pacific Humpback (Sousa chinensis) Dolphins in North-Western Australia 
PLoS ONE  2014;9(7):e101427.
Little is known about the Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa chinensis) dolphins (‘snubfin’ and ‘humpback dolphins’, hereafter) of north-western Australia. While both species are listed as ‘near threatened’ by the IUCN, data deficiencies are impeding rigorous assessment of their conservation status across Australia. Understanding the genetic structure of populations, including levels of gene flow among populations, is important for the assessment of conservation status and the effective management of a species. Using nuclear and mitochondrial DNA markers, we assessed population genetic diversity and differentiation between snubfin dolphins from Cygnet (n = 32) and Roebuck Bays (n = 25), and humpback dolphins from the Dampier Archipelago (n = 19) and the North West Cape (n = 18). All sampling locations were separated by geographic distances >200 km. For each species, we found significant genetic differentiation between sampling locations based on 12 (for snubfin dolphins) and 13 (for humpback dolphins) microsatellite loci (FST = 0.05–0.09; P<0.001) and a 422 bp sequence of the mitochondrial control region (FST = 0.50–0.70; P<0.001). The estimated proportion of migrants in a population ranged from 0.01 (95% CI 0.00–0.06) to 0.13 (0.03–0.24). These are the first estimates of genetic diversity and differentiation for snubfin and humpback dolphins in Western Australia, providing valuable information towards the assessment of their conservation status in this rapidly developing region. Our results suggest that north-western Australian snubfin and humpback dolphins may exist as metapopulations of small, largely isolated population fragments, and should be managed accordingly. Management plans should seek to maintain effective population size and gene flow. Additionally, while interactions of a socio-sexual nature between these two species have been observed previously, here we provide strong evidence for the first documented case of hybridisation between a female snubfin dolphin and a male humpback dolphin.
doi:10.1371/journal.pone.0101427
PMCID: PMC4079686  PMID: 24988113
14.  Behavioural Effects of Tourism on Oceanic Common Dolphins, Delphinus sp., in New Zealand: The Effects of Markov Analysis Variations and Current Tour Operator Compliance with Regulations 
PLoS ONE  2015;10(1):e0116962.
Common dolphins, Delphinus sp., are one of the marine mammal species tourism operations in New Zealand focus on. While effects of cetacean-watching activities have previously been examined in coastal regions in New Zealand, this study is the first to investigate effects of commercial tourism and recreational vessels on common dolphins in an open oceanic habitat. Observations from both an independent research vessel and aboard commercial tour vessels operating off the central and east coast Bay of Plenty, North Island, New Zealand were used to assess dolphin behaviour and record the level of compliance by permitted commercial tour operators and private recreational vessels with New Zealand regulations. Dolphin behaviour was assessed using two different approaches to Markov chain analysis in order to examine variation of responses of dolphins to vessels. Results showed that, regardless of the variance in Markov methods, dolphin foraging behaviour was significantly altered by boat interactions. Dolphins spent less time foraging during interactions and took significantly longer to return to foraging once disrupted by vessel presence. This research raises concerns about the potential disruption to feeding, a biologically critical behaviour. This may be particularly important in an open oceanic habitat, where prey resources are typically widely dispersed and unpredictable in abundance. Furthermore, because tourism in this region focuses on common dolphins transiting between adjacent coastal locations, the potential for cumulative effects could exacerbate the local effects demonstrated in this study. While the overall level of compliance by commercial operators was relatively high, non-compliance to the regulations was observed with time restriction, number or speed of vessels interacting with dolphins not being respected. Additionally, prohibited swimming with calves did occur. The effects shown in this study should be carefully considered within conservation management plans, in order to reduce the risk of detrimental effects on common dolphins within the region.
doi:10.1371/journal.pone.0116962
PMCID: PMC4286237  PMID: 25565523
15.  The Ecological Conditions That Favor Tool Use and Innovation in Wild Bottlenose Dolphins (Tursiops sp.) 
PLoS ONE  2011;6(7):e22243.
Dolphins are well known for their exquisite echolocation abilities, which enable them to detect and discriminate prey species and even locate buried prey. While these skills are widely used during foraging, some dolphins use tools to locate and extract prey. In the only known case of tool use in free-ranging cetaceans, a subset of bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia habitually employs marine basket sponge tools to locate and ferret prey from the seafloor. While it is clear that sponges protect dolphins' rostra while searching for prey, it is still not known why dolphins probe the substrate at all instead of merely echolocating for buried prey as documented at other sites. By ‘sponge foraging’ ourselves, we show that these dolphins target prey that both lack swimbladders and burrow in a rubble-littered substrate. Delphinid echolocation and vision are critical for hunting but less effective on such prey. Consequently, if dolphins are to access this burrowing, swimbladderless prey, they must probe the seafloor and in turn benefit from using protective sponges. We suggest that these tools have allowed sponge foraging dolphins to exploit an empty niche inaccessible to their non-tool-using counterparts. Our study identifies the underlying ecological basis of dolphin tool use and strengthens our understanding of the conditions that favor tool use and innovation in the wild.
doi:10.1371/journal.pone.0022243
PMCID: PMC3140497  PMID: 21799801
16.  Comparative Analysis of Three Brevetoxin-Associated Bottlenose Dolphin (Tursiops truncatus) Mortality Events in the Florida Panhandle Region (USA) 
PLoS ONE  2012;7(8):e42974.
In the Florida Panhandle region, bottlenose dolphins (Tursiops truncatus) have been highly susceptible to large-scale unusual mortality events (UMEs) that may have been the result of exposure to blooms of the dinoflagellate Karenia brevis and its neurotoxin, brevetoxin (PbTx). Between 1999 and 2006, three bottlenose dolphin UMEs occurred in the Florida Panhandle region. The primary objective of this study was to determine if these mortality events were due to brevetoxicosis. Analysis of over 850 samples from 105 bottlenose dolphins and associated prey items were analyzed for algal toxins and have provided details on tissue distribution, pathways of trophic transfer, and spatial-temporal trends for each mortality event. In 1999/2000, 152 dolphins died following extensive K. brevis blooms and brevetoxin was detected in 52% of animals tested at concentrations up to 500 ng/g. In 2004, 105 bottlenose dolphins died in the absence of an identifiable K. brevis bloom; however, 100% of the tested animals were positive for brevetoxin at concentrations up to 29,126 ng/mL. Dolphin stomach contents frequently consisted of brevetoxin-contaminated menhaden. In addition, another potentially toxigenic algal species, Pseudo-nitzschia, was present and low levels of the neurotoxin domoic acid (DA) were detected in nearly all tested animals (89%). In 2005/2006, 90 bottlenose dolphins died that were initially coincident with high densities of K. brevis. Most (93%) of the tested animals were positive for brevetoxin at concentrations up to 2,724 ng/mL. No DA was detected in these animals despite the presence of an intense DA-producing Pseudo-nitzschia bloom. In contrast to the absence or very low levels of brevetoxins measured in live dolphins, and those stranding in the absence of a K. brevis bloom, these data, taken together with the absence of any other obvious pathology, provide strong evidence that brevetoxin was the causative agent involved in these bottlenose dolphin mortality events.
doi:10.1371/journal.pone.0042974
PMCID: PMC3419745  PMID: 22916189
17.  Stereology of the Thyroid Gland in Indo-Pacific Bottlenose Dolphin (Tursiops aduncus) in Comparison with Human (Homo sapiens): Quantitative and Functional Implications 
PLoS ONE  2013;8(5):e62060.
The mammalian thyroid gland maintains basal metabolism in tissues for optimal function. Determining thyroid volume is important in assessing growth and involution. Volume estimation is also important in stereological studies. Direct measurements of colloid volume and nuclear-to-cytoplasmic ratio of the follicular cells may provide important information about thyroid gland function such as hormone storage and secretion, which helps understand the changes at morphological and functional levels. The present study determined the colloid volume using simple stereological principle and the nuclear-to-cytoplasmic ratio of 4 Indo-Pacific bottlenose dolphins and 2 human thyroid glands. In both dolphin and human thyroid glands, the size of the follicles tended to be quite variable. The distribution of large and small follicles within the thyroid gland was also found to be random in both the dolphin and human thyroid gland; however, the size of follicles appeared to decrease as a function of increasing age in the dolphin thyroid gland. The mean colloid volume of the dolphin thyroid gland and human thyroid gland was 1.22×105 µm3 and 7.02×105 µm3 respectively. The dolphin and human subjects had a significant difference in the mean colloid volume. The mean N/C ratio of the dolphin thyroid follicular epithelia and human follicular epithelia was 0.50 and 0.64 respectively. The dolphin and human subjects had a significant difference in the mean N/C ratio. This information contributes to understanding dolphin thyroid physiology and its structural adaptations to meet the physical demands of the aquatic environment, and aids with ultrasonography and corrective therapy in live subjects.
doi:10.1371/journal.pone.0062060
PMCID: PMC3653896  PMID: 23690927
18.  The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen 
Biology Letters  2012;8(5):702-705.
Diverse and localized foraging behaviours have been reported in isolated populations of many animal species around the world. In Laguna, southern Brazil, a subset of resident bottlenose dolphins (Tursiops truncatus) uses a foraging tactic involving cooperative interactions with local, beach-casting fishermen. We used individual photo-identification data to assess whether cooperative and non-cooperative dolphins were socially segregated. The social structure of the population was found to be a fission–fusion system with few non-random associations, typical for this species. However, association values were greater among cooperative dolphins than among non-cooperative dolphins or between dolphins from different foraging classes. Furthermore, the dolphin social network was divided into three modules, clustering individuals that shared or lacked the cooperative foraging tactic. Space-use patterns were not sufficient to explain this partitioning, indicating a behavioural factor. The segregation of dolphins using different foraging tactics could result from foraging behaviour driving social structure, while the closer association between dolphins engaged in the cooperation could facilitate the transmission and learning of this behavioural trait from conspecifics. This unique case of a dolphin–human interaction represents a valuable opportunity to explore hypotheses on the role of social learning in wild cetaceans.
doi:10.1098/rsbl.2012.0174
PMCID: PMC3440962  PMID: 22552635
Tursiops truncatus; cooperative behaviour; artisanal fishermen; foraging tactics; social learning
19.  A Mini Review of Dolphin Carbohydrate Metabolism and Suggestions for Future Research Using Exhaled Air 
In the 1960s, I explored some aspects of carbohydrate metabolism in healthy bottlenose dolphins (Tursiops truncatus). Their physiological picture resembled what had been described for hyperthyroid diabetics. Dolphins have elevated thyroid hormone turnover, and fasting dolphins maintain a relatively high level of plasma glucose. After dolphins ingest glucose, plasma levels remain high for many hours. Interestingly, plasma glucose must exceed 300 mg/dL (about twice as high as the human threshold) before glucose appears in urine. Due to their diabetes-like states, trainability, and unique natural respiratory anatomy and physiology, dolphins may offer useful clues to metabolites in the breath that may be used to non-invasively monitor diabetes in humans. Dolphins take very rapid and deep breaths that are four or five times as deep as humans and other terrestrial mammals, making them ideal for physiological assessment using non-invasive exhaled air. Avenues for successfully identifying breath-based markers for metabolic disease and physiology in dolphins can be done with both modern technology and the evolutionarily advantageous canine nose. This review summarizes aspects of dolphin metabolism previously learned and offers new directions for diabetes research that may benefit both dolphin and human health.
doi:10.3389/fendo.2013.00152
PMCID: PMC3863911  PMID: 24379802
dolphin; carbohydrate; breath analysis; diabetes; exhalation; glucose; dog; smell
20.  Demographic Clusters Identified within the Northern Gulf of Mexico Common Bottlenose Dolphin (Tursiops truncates) Unusual Mortality Event: January 2010 - June 2013 
PLoS ONE  2015;10(2):e0117248.
A multi-year unusual mortality event (UME) involving primarily common bottlenose dolphins (Tursiops truncates) was declared in the northern Gulf of Mexico (GoM) with an initial start date of February 2010 and remains ongoing as of August 2014. To examine potential changing characteristics of the UME over time, we compared the number and demographics of dolphin strandings from January 2010 through June 2013 across the entire GoM as well as against baseline (1990-2009) GoM stranding patterns. Years 2010 and 2011 had the highest annual number of stranded dolphins since Louisiana’s record began, and 2011 was one of the years with the highest strandings for both Mississippi and Alabama. Statewide, annual numbers of stranded dolphins were not elevated for GoM coasts of Florida or Texas during the UME period. Demographic, spatial, and temporal clusters identified within this UME included increased strandings in northern coastal Louisiana and Mississippi (March-May 2010); Barataria Bay, Louisiana (August 2010-December 2011); Mississippi and Alabama (2011, including a high prevalence and number of stranded perinates); and multiple GoM states during early 2013. While the causes of the GoM UME have not been determined, the location and magnitude of dolphin strandings during and the year following the 2010 Deepwater Horizon oil spill, including the Barataria Bay cluster from August 2010 to December 2011, overlap in time and space with locations that received heavy and prolonged oiling. There are, however, multiple known causes of previous GoM dolphin UMEs, including brevetoxicosis and dolphin morbillivirus. Additionally, increased dolphin strandings occurred in northern Louisiana and Mississippi before the Deepwater Horizon oil spill. Identification of spatial, temporal, and demographic clusters within the UME suggest that this mortality event may involve different contributing factors varying by location, time, and bottlenose dolphin populations that will be better discerned by incorporating diagnostic information, including histopathology.
doi:10.1371/journal.pone.0117248
PMCID: PMC4324990  PMID: 25671657
21.  Isolation and Characterization of a Helicobacter sp. from the Gastric Mucosa of Dolphins, Lagenorhynchus acutus and Delphinus delphis 
Applied and Environmental Microbiology  2000;66(11):4751-4757.
Gastric ulcerations in dolphins have been reported for decades. Some of these lesions were associated with parasitic infections. However, cases of nonparasitic gastric ulcers with no clearly defined etiology also have been reported in wild and captive dolphins. Considerable speculation exists as to whether dolphins have Helicobacter-associated gastritis and peptic ulcer disease. The stomachs of seven stranded Atlantic white-sided dolphins, Lagenorhynchus acutus, and 1 common dolphin, Delphinus delphis, were assessed for the presence of Helicobacter species. Novel Helicobacter species were identified by culture in the gastric mucosa of two of the eight dolphins studied and by PCR in seven of the eight dolphins. The gram-negative organisms were urease, catalase, and oxidase positive. Spiral to fusiform bacteria were detected in gastric mucosa by Warthin Starry staining. Histopathology revealed mild to moderate diffuse lymphoplasmacytic gastritis within the superficial mucosa of the main stomach. The pyloric stomach was less inflamed, and bacteria did not extend deep into the glands. The lesions parallel those observed in Helicobacter pylori-infected humans. Bacteria from two dolphins classified by 16S rRNA analysis clustered with gastric helicobacters and represent a novel Helicobacter sp. most closely related to H. pylori. These findings suggest that a novel Helicobacter sp. may play a role in the etiopathogenesis of gastritis and gastric ulcers in dolphins. To our knowledge this represents the first isolation and characterization of a novel Helicobacter sp. from a marine mammal and emphasizes the wide host distribution and pathogenic potential of this increasingly important genus.
PMCID: PMC92375  PMID: 11055919
22.  STUDIES ON THE INTERMEDIARY CARBOHYDRATE METABOLISM OF AQUATIC ANIMALS  
The Journal of General Physiology  1948;31(4):347-359.
1. Liver, kidney, brain, skeletal muscle, and cardiac muscle from one newborn and three adult long-snouted dolphins (Stenella plagiodon) were obtained for enzyme studies. 2. All of the dolphin tissues exhibited cytochrome oxidase, succinic dehydrogenase, and malic dehydrogenase activity. Considerable differences in the enzyme activities of the various tissues were noted, with cardiac muscle exhibiting the highest respiratory enzyme activity. The enzyme activities of dolphin tissues were lower than those of the corresponding rat tissues. 3. All of the dolphin tissues exhibited adenosine triphosphatase activity which was accelerated by magnesium and manganese but, in contrast to rat tissues, was only slightly activated by calcium. 4. Measurements of the distribution of acid-soluble phosphorus in dolphin tissues indicated that glycolysis in all of the tissues examined proceeded through the Emden-Meyerhof phosphorylation scheme. 5. The average glycogen content of dolphin skeletal muscle was 0.98 per cent as compared with 0.16 to 0.20 per cent for rat skeletal muscle. The high glycogen content of dolphin skeletal muscle indicates a ready source of substrate for glycolysis even during submergence when the blood supply may be differentially shunted to other organs. 6. Measurements of the organ weights of dolphins showed that the lungs occupy over three times and the liver one-half as much of the total body weight as do these organs in the rat. The heart and the thyroid gland of the dolphin are also larger in proportion to the total body weight than in the rat while the relative weights of the other tissues in the two species are about the same.
PMCID: PMC2147112  PMID: 18904758
23.  Detection of Canine Distemper Virus Nucleoprotein RNA by Reverse Transcription-PCR Using Serum, Whole Blood, and Cerebrospinal Fluid from Dogs with Distemper 
Journal of Clinical Microbiology  1999;37(11):3634-3643.
Reverse transcription-PCR (RT-PCR) was used to detect canine distemper virus (CDV) nucleoprotein (NP) RNA in serum, whole blood, and cerebrospinal fluid (CSF) samples from 38 dogs with clinically suspected distemper. Results were correlated to clinical findings, anti-CDV neutralizing antibody titers, postmortem findings, and demonstration of CDV NP antigen by immunohistochemistry. The specificity of the RT-PCR was ensured by amplification of RNA from various laboratory CDV strains, restriction enzyme digestion, and Southern blot hybridization. In 29 of 38 dogs, CDV infection was confirmed by postmortem examination and immunohistochemistry. The animals displayed the catarrhal, systemic, and nervous forms of distemper. Seventeen samples (serum, whole blood, or CSF) from dogs with distemper were tested with three sets of primers targeted to different regions of the NP gene of the CDV Onderstepoort strain. Expected amplicons were observed in 82, 53, and 41% of the 17 samples, depending upon the primer pair used. With the most sensitive primer pair (primer pair I), CDV NP RNA was detected in 25 of 29 (86%) serum samples and 14 of 16 (88%) whole blood and CSF samples from dogs with distemper but not in body fluids from immunohistochemically negative dogs. Nucleotide sequence analysis of five RT-PCR amplicons from isolates from the field revealed few silent point mutations. These isolates exhibited greater homology to the Rockborn (97 to 99%) than to the Onderstepoort (95 to 96%) CDV strain. In summary, although the sensitivity of the RT-PCR for detection of CDV is strongly influenced by the location of the selected primers, this nucleic acid detection system represents a highly specific and sensitive method for the antemortem diagnosis of distemper in dogs, regardless of the form of distemper, humoral immune response, and viral antigen distribution.
PMCID: PMC85712  PMID: 10523566
24.  Concurrent Exposure of Bottlenose Dolphins (Tursiops truncatus) to Multiple Algal Toxins in Sarasota Bay, Florida, USA 
PLoS ONE  2011;6(3):e17394.
Sentinel species such as bottlenose dolphins (Tursiops truncatus) can be impacted by large-scale mortality events due to exposure to marine algal toxins. In the Sarasota Bay region (Gulf of Mexico, Florida, USA), the bottlenose dolphin population is frequently exposed to harmful algal blooms (HABs) of Karenia brevis and the neurotoxic brevetoxins (PbTx; BTX) produced by this dinoflagellate. Live dolphins sampled during capture-release health assessments performed in this region tested positive for two HAB toxins; brevetoxin and domoic acid (DA). Over a ten-year study period (2000–2009) we have determined that bottlenose dolphins are exposed to brevetoxin and/or DA on a nearly annual basis (i.e., DA: 2004, 2005, 2006, 2008, 2009; brevetoxin: 2000, 2004, 2005, 2008, 2009) with 36% of all animals testing positive for brevetoxin (n = 118) and 53% positive for DA (n = 83) with several individuals (14%) testing positive for both neurotoxins in at least one tissue/fluid. To date there have been no previously published reports of DA in southwestern Florida marine mammals, however the May 2008 health assessment coincided with a Pseudo-nitzschia pseudodelicatissima bloom that was the likely source of DA observed in seawater and live dolphin samples. Concurrently, both DA and brevetoxin were observed in common prey fish. Although no Pseudo-nitzschia bloom was identified the following year, DA was identified in seawater, fish, sediment, snails, and dolphins. DA concentrations in feces were positively correlated with hematologic parameters including an increase in total white blood cell (p = 0.001) and eosinophil (p<0.001) counts. Our findings demonstrate that dolphins within Sarasota Bay are commonly exposed to two algal toxins, and provide the impetus to further explore the potential long-term impacts on bottlenose dolphin health.
doi:10.1371/journal.pone.0017394
PMCID: PMC3053359  PMID: 21423740
25.  Predictive Modeling of Spinner Dolphin (Stenella longirostris) Resting Habitat in the Main Hawaiian Islands 
PLoS ONE  2012;7(8):e43167.
Predictive habitat models can provide critical information that is necessary in many conservation applications. Using Maximum Entropy modeling, we characterized habitat relationships and generated spatial predictions of spinner dolphin (Stenella longirostris) resting habitat in the main Hawaiian Islands. Spinner dolphins in Hawai'i exhibit predictable daily movements, using inshore bays as resting habitat during daylight hours and foraging in offshore waters at night. There are growing concerns regarding the effects of human activities on spinner dolphins resting in coastal areas. However, the environmental factors that define suitable resting habitat remain unclear and must be assessed and quantified in order to properly address interactions between humans and spinner dolphins. We used a series of dolphin sightings from recent surveys in the main Hawaiian Islands and a suite of environmental variables hypothesized as being important to resting habitat to model spinner dolphin resting habitat. The model performed well in predicting resting habitat and indicated that proximity to deep water foraging areas, depth, the proportion of bays with shallow depths, and rugosity were important predictors of spinner dolphin habitat. Predicted locations of suitable spinner dolphin resting habitat provided in this study indicate areas where future survey efforts should be focused and highlight potential areas of conflict with human activities. This study provides an example of a presence-only habitat model used to inform the management of a species for which patterns of habitat availability are poorly understood.
doi:10.1371/journal.pone.0043167
PMCID: PMC3427338  PMID: 22937022

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