Unique seasonal forage bases within a local population of bottlenose dolphin (Tursiops truncatus)

Using photo‐identification data, bottlenose dolphin (Tursiops truncatus) populations can be differentiated based on their use of particular estuaries or coastal habitats. Questions remain, however, about the validity of such fine‐scale population partitioning and whether the resulting assemblages utilize unique forage bases. To address the issue of forage base use, stable isotopes of carbon (δ¹³C), nitrogen (δ¹⁵N) and sulfur (δ³⁴S) were analyzed from skin tissues (n= 74) of bottlenose dolphins sampled seasonally along the coast and in three estuaries near Charleston, South Carolina. Autumn values of δ³⁴S, δ¹⁵N, and δ¹³C and summer values of δ³⁴S indicated that dolphins sampled from these four assemblages utilized unique forage bases, despite limited sample sizes. Likewise, autumn and spring differences in δ¹⁵N and δ¹³C values were evident in the North Edisto River, and in δ³⁴S from dolphins sampled from all three estuarine assemblages; no seasonal differences were identified in the coastal assemblage. Results demonstrate the importance of considering spatial and temporal variation in forage base when developing local management plans for bottlenose dolphin and highlight the discriminatory power of δ³⁴S for estuarine and coastal marine mammals. These results also suggest that stable isotopes could be developed as a complementary tool for photo‐identification based partitioning of bottlenose dolphin populations.     

Stable isotopes differentiate bottlenose dolphins off west-central Florida

Distinguishing discrete population units among continuously distributed coastal small cetaceans is challenging and crucial to conservation. We evaluated the utility of stable isotopes in assessing group membership in bottlenose dolphins (Tursiops truncatus) off west-central Florida by analyzing carbon, nitrogen, and sulfur isotope values (δ¹³C, δ¹⁵N, and δ³⁴S) of tooth collagen from stranded dolphins. Individuals derived from three putative general population units: Sarasota Bay (SB), nearshore Gulf of Mexico (GULF), and offshore waters (OFF). Animals of known history (SB) served to ground truth the approach against animals of unknown history from the Gulf of Mexico (GULF, OFF). Dolphin groups differed significantly for each isotope. Average δ¹³C values from SB dolphins (−10.6‰) utilizing sea grass ecosystems differed from those of GULF (−11.9‰) and OFF (−11.9‰). Average δ¹⁵N values of GULF (12.7‰) and OFF (13.2‰) were higher than those of SB dolphins (11.9‰), consistent with differences in prey trophic levels. δ³⁴S values showed definitive differences among SB (7.1‰), GULF (11.3‰), and OFF (16.5‰) dolphins. This is the first application of isotopes to population assignment of bottlenose dolphins in the Gulf of Mexico and results suggest that isotopes may provide a powerful tool in the conservation of small cetaceans.     

Feeding ecology of the highly threatened common bottlenose dolphin of the Gulf of Ambracia,Greece, through stable isotope analysis

The Gulf of Ambracia, in northwestern Greece, hosts a highly threatened community of about 150 common bottlenose dolphins (Tursiops truncatus). Until now, information on their feeding habits was derived exclusively from fish scale samples collected during surface-feeding events targeting small schooling epipelagic fish. The aim of this study was to determine the diet of bottlenose dolphins living in the Gulf of Ambracia through the application of Bayesian isotopic mixing models. Skin biopsy samples of 16 dolphins were analyzed and no difference related to sex or age-class was found in δ¹³C and δ¹⁵N values. Results suggested that the dolphin diet was mainly based on Trachurus trachurus, species belonging to the family Sparidae: Diplodus annularis, Lithognathus mormyrus, and Sepia officinalis, which represented together about 42% ± 15% of the biomass ingested, followed by species belonging to the order Clupeiformes (Engraulis encrasicolus, Sardinella aurita, and Sardina pilchardus) and the genus Gobius (37% ± 17%). A better understanding of the feeding habits of these dolphins sheds light on the feeding ecology of this highly threatened population by, for instance, evidencing interactions with artisanal fisheries sharing the same target species, and is key for identifying adequate management measures consistent with an ecosystem-based approach.     

Niche overlap and diet composition of three sympatric coastal dolphin species in the southwest Atlantic Ocean

Sympatric species are expected to differ in ecological requirements to minimize niche overlap and avoid competition. Here we assess the trophic interactions among three coexisting dolphin species from southern Brazil: the franciscana dolphin (Pontoporia blainvillei), the Guiana dolphin (Sotalia guianensis), and the Lahille's bottlenose dolphin (Tursiops truncatus gephyreus). We evaluated temporal variation in carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values of bone collagen to examine potential dietary shifts resulting from increased fishing activity over the past three decades. We estimated the degree of niche overlap among these species and the contribution of potential prey sources to their diet. δ¹⁵N values were consistent among species and across years, while δ¹³C values increased for Guiana dolphins and decreased for bottlenose dolphins, suggesting changes in diet and/or foraging habitats through time. The similar δ¹³C and δ¹⁵N values and the high niche overlap between Guiana and bottlenose dolphins indicate that these species are primarily feeding on demersal prey. The franciscana diet is primarily composed of pelagic prey, resulting in a lower niche overlap in comparison with the other dolphin species. Our study provides further information about the foraging ecology of this unique dolphin community in southern Brazil with implications for its management and conservation.     

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.     

Genetic isolation between coastal and fishery‐impacted,offshore bottlenose dolphin (Tursiops spp.) populations

The identification of species and population boundaries is important in both evolutionary and conservation biology. In recent years, new population genetic and computational methods for estimating population parameters and testing hypotheses in a quantitative manner have emerged. Using a Bayesian framework and a quantitative model‐testing approach, we evaluated the species status and genetic connectedness of bottlenose dolphin (Tursiops spp.) populations off remote northwestern Australia, with a focus on pelagic ‘offshore’ dolphins subject to incidental capture in a trawl fishery. We analysed 71 dolphin samples from three sites beyond the 50 m depth contour (the inshore boundary of the fishery) and up to 170 km offshore, including incidentally caught and free‐ranging individuals associating with trawl vessels, and 273 dolphins sampled at 12 coastal sites inshore of the 50 m depth contour and within 10 km of the coast. Results from 19 nuclear microsatellite markers showed significant population structure between dolphins from within the fishery and coastal sites, but also among dolphins from coastal sites, identifying three coastal populations. Moreover, we found no current or historic gene flow into the offshore population in the region of the fishery, indicating a complete lack of recruitment from coastal sites. Mitochondrial DNA corroborated our findings of genetic isolation between dolphins from the offshore population and coastal sites. Most offshore individuals formed a monophyletic clade with common bottlenose dolphins (T. truncatus), while all 273 individuals sampled coastally formed a well‐supported clade of Indo‐Pacific bottlenose dolphins (T. aduncus). By including a quantitative modelling approach, our study explicitly took evolutionary processes into account for informing the conservation and management of protected species. As such, it may serve as a template for other, similarly inaccessible study populations.     

Genetic divergence between two phenotypically distinct bottlenose dolphin ecotypes suggests separate evolutionary trajectories

Due to their worldwide distribution and occupancy of different types of environments, bottlenose dolphins display considerable morphological variation. Despite limited understanding about the taxonomic identity of such forms and connectivity among them at global scale, coastal (or inshore) and offshore (or oceanic) ecotypes have been widely recognized in several ocean regions. In the Southwest Atlantic Ocean (SWA), however, there are scarce records of bottlenose dolphins differing in external morphology according to habitat preferences that resemble the coastal‐offshore pattern observed elsewhere. The main aim of this study was to analyze the genetic variability, and test for population structure between coastal (n = 127) and offshore (n = 45) bottlenose dolphins sampled in the SWA to assess whether their external morphological distinction is consistent with genetic differentiation. We used a combination of mtDNA control region sequences and microsatellite genotypes to infer population structure and levels of genetic diversity. Our results from both molecular marker types were congruent and revealed strong levels of structuring (microsatellites F_ST = 0.385, p < .001; mtDNA F_ST =  0.183, p < .001; Φ_ST = 0.385, p < .001) and much lower genetic diversity in the coastal than the offshore ecotype, supporting patterns found in previous studies elsewhere. Despite the opportunity for gene flow in potential “contact zones”, we found minimal current and historical connectivity between ecotypes, suggesting they are following discrete evolutionary trajectories. Based on our molecular findings, which seem to be consistent with morphological differentiations recently described for bottlenose dolphins in our study area, we recommend recognizing the offshore bottlenose dolphin ecotype as an additional Evolutionarily Significant Unit (ESU) in the SWA. Implications of these results for the conservation of bottlenose dolphins in SWA are also discussed.     

MORBILLIVIRUS INFECTION IN BOTTLENOSE DOLPHINS: EVIDENCE FOR RECURRENT EPIZOOTICS IN THE WESTERN ATLANTIC AND GULF OF MEXICO

Morbillivirus infection is widespread among odontocetes of the western Atlantic and Gulf of Mexico. Serologic evidence of infection in bottlenose dolphins, Tursiops truncatus , was first detected during an epizootic along the mid-Atlantic coast in 1987. Here, we report recurrent epizootics in the coastal dolphin population since at least the early 1980s based on serological surveys and regional stranding frequencies. The first observed epizootic of this series occurred in the Indian and Banana Rivers in 1982 and was followed by others on the mid-Atlantic coast in 1987–1988 and in the Gulf of Mexico between 1992 and 1994. This temporal pattern of infection is likely facilitated by the population size and its fragmentation into relatively discrete coastal communities. Introduction of morbillivirus into a community with a sufficient number of naive hosts may precipitate an epizootic, depending on the potential for transmission within the group. Propagation of an epizootic along the coast is probably determined by frequency of contact between adjacent communities and seasonal migrations.
Morbillivirus antibodies were also detected in serum from offshore bottlenose dolphins. The sero-prevalence in the latter may be higher than in coastal dolphins because of their close association with enzootically infected pilot whales ( Globicephala spp.). Occasional contact between offshore and coastal dolphins may provide an epizootiologic link between pilot whales and coastal dolphin communities.     

Feeding aggregation and aggressive interaction between bottlenose (Tursiops truncatus) and Commerson’s dolphins (Cephalorhynchus commersonii) in Patagonia,Argentina

We report the first recorded interactions between bottlenose dolphin (Tursiops truncatus) and Commerson’s dolphins (Cephalorhynchus commersonii). The diurnal behavioral patterns of bottlenose dolphins in Bahía Engaño, Argentina, were similar to those described for other coastal populations around the world. The majority of the feeding bouts were recorded near the mouth the Chubut River. When not feeding near the river, bottlenose dolphins generally swam along the coast, and interactions with Commerson’s dolphins were recorded very close to the shore on two occasions during a 3-year period. In the first event, both species were feeding on a fish school. The second interaction was aggressive in nature, involving one juvenile and three adult bottlenose dolphins with several Commerson’s dolphins. Two of the adult bottlenose dolphins attacked the Commerson’s dolphins. We propose that the observed behavior represented defense of the juvenile bottlenose dolphin.

     

STABLE ISOTOPE ANALYSES OF TOOTH ANNULI REVEAL TEMPORAL DIETARY RECORDS: AN EXAMPLE USING STELLER SEA LIONS

Stable isotope analysis of teeth of marine mammals can provide valuable information on trophic level and source of feeding. However, the isotopic analysis of whole teeth presents only an average dietary estimate for individuals across the period of growth of that tooth. While such analyses can be valuable, particularly in the case of fossil material, in contrast, isotopic analysis of individual annuli of teeth can provide dietary information for each year of tooth growth, in some cases representing the whole of the animal's life. We measured stable-carbon isotope ratios (¹³C/¹²C) in the inorganic (hydroxyapatite) and stable-nitrogen isotope ratios (¹⁵N/¹⁴N) in the organic (primarily collagenous) components of individual tooth annuli of 18 male Steller sea lions (Eumetopias jubatus) obtained from archived collections from the Bering Sea and Gulf of Alaska and from single northern fur seals (Callorbinus ursinus) and northern elephant seals (Mirounga angustirostris) from the central Aleutian Islands and eastern Gulf of Alaska, respectively. In several individuals, we detected considerable variation in stable isotope values among annuli, up to 6.1%_O for δ¹⁵N and 5.1%_O for δ¹³C values. Enrichment in δ¹⁵N and depletion of δ¹³C values in the first annulus may correspond to dietary inputs from mother's milk during the period of suckling. Other variations among years may be caused by dietary changes or movements of individuals between regions differing in isotopic signatures of foodweb primary production. Our study indicates that the isotopic signatures of foodweb primary production. Our study indicates that the isotopic analysis of individual tooth annuli represents a fine-seale tool for dietary reconstructions involving marine mammals, and cautions against the use of whole-tooth material averaged over several annuli.     

DIETARY STUDIES OF MARINE MAMMALS USING STABLE CARBON AND NITROGEN ISOTOPIC RATIOS OF TEETH

This study used naturally occurring carbon and nitrogen stable isotopes of teeth to study the diets of marine mammals. The isotopic ratios of nonchemically preserved teeth from eight species of marine mammals, representing 87 individuals that spanned the trophic continuum, were found to reflect nutritional sources. The δ¹³C signals distinguished animals that lived in waters dominated by different primary producers (e. g., seagrass, kelp, and phytoplankton), and δ¹⁵N values indicated the diet and trophic level of the species. This research suggests that isotopic signatures of teeth can be used in dietary studies to show differences and similarities among age classes, genders, geographic locations, and time periods.     

Differences in acoustic signals from Delphinids in the western North Atlantic and northern Gulf of Mexico

Whistle characteristics were quantitatively compared between both geographically separated and neighboring populations of Atlantic spotted dolphins (Stenella frontalis), bottlenose dolphins (Tursiops truncatus), and pilot whales (Globicephala spp.) in U.S. waters to evaluate if intraspecific acoustic differences exist between groups. We compared nine whistle characteristics between continental shelf and offshore Atlantic spotted dolphins in the western North Atlantic and between northern Gulf of Mexico and western North Atlantic bottlenose dolphins and pilot whales using discriminant analysis. Offshore Atlantic spotted dolphin whistles were significantly different (Hotelling's T², P= 0.0003) from continental shelf whistles in high frequency, bandwidth, duration, number of steps, and number of inflection points. Atlantic bottlenose dolphin whistles were significantly different (Hotelling's T², P < 0.0001) from those in the Gulf of Mexico in duration, number of steps, and number of inflection points. There was no significant difference between pilot whale whistles in the two basins. The whistle differences indicate acoustic divergence between groups in different areas that may arise from geographic isolation or habitat separation between neighboring but genetically distinct populations of dolphins. This study supports the premise that acoustic differences can be a tool to evaluate the ecological separation between marine mammal groups in field studies.     

IMPROVING MANAGEMENT OF OVERLAPPING BOTTLENOSE DOLPHIN ECOTYPES THROUGH SPATIAL ANALYSIS AND GENETICS

In the Northwest Atlantic the distribution of coastal bottlenose dolphins ( Tursiops truncatus ) overlaps with that of the offshore ecotype. We hypothesized that the distribution of the two ecotypes could be delineated by depth and/or distance from shore, facilitating their identification during surveys. We obtained 304 skin biopsy samples and identified each as either coastal or offshore using analysis of mitochondrial DNA. We then interpreted the spatial distribution of coastal and offshore forms using spatial analysis. Using a Classification and Regression Tree (CART) analysis, we found a statistically significant break in ecotype distribution at 34 km from shore. In waters beyond 34 km from shore and deeper than 34 m, all bottlenose dolphins were of the offshore ecotype. Within 7.5 km of shore, all 65 samples were of the coastal ecotype. Between these two areas only nine samples were collected, so the genetic composition of bottlenose dolphins in this area remains poorly known. To enhance our understanding of the spatial distribution of the two ecotypes, future research should obtain more biopsy samples in this zone. Nevertheless, our results indicate that a conservative abundance estimate for the coastal ecotype could be generated from surveys of bottlenose dolphins within 7.5 km of shore.     

Integrating multiple data sources to assess the distribution and abundance of bottlenose dolphins Tursiops truncatus in Scottish waters

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Spatio‐temporal isotopic signatures (δ13C and δ15N) reveal that two sympatric West African mullet species do not feed on the same basal production sources

Potential trophic competition between two sympatric mullet species, Mugil cephalus and Mugil curema, was explored in the hypersaline estuary of the Saloum Delta (Senegal) using δ¹³C and δ¹⁵N composition of muscle tissues. Between species, δ¹⁵N compositions were similar, suggesting a similar trophic level, while the difference in δ¹³C compositions indicated that these species did not feed from exactly the same basal production sources or at least not in the same proportions. This result provides the first evidence of isotopic niche segregation between two limno‐benthophageous species belonging to the geographically widespread, and often locally abundant, Mugilidae family.     

Genetic differentiation among coastal and offshore common bottlenose dolphins,Tursiops truncatus,in the eastern North Pacific Ocean

Common bottlenose dolphins (Tursiops truncatus) are found worldwide in temperate and tropical regions, often occurring as distinct coastal and offshore ecotypes. Along the west coast of the United States, two stocks are recognized for management based on morphological and photo‐identification studies: a California coastal stock, estimated at 450–500 individuals, and a California/Oregon/Washington offshore stock of about 1,000 animals. This study is the first to analyze genetic differentiation between these stocks. We examined both the hypervariable portion of the mitochondrial DNA (mtDNA) control region and fifteen microsatellite markers for coastal (n = 64) and offshore (n = 69) dolphins. Significant genetic differentiation was found between the two stocks for mtDNA (Φ_ST = 0.30, P < 0.001; F_ST = 0.14, P < 0.001) and microsatellite loci (F_ST = 0.19, P < 0.001). Coastal dolphins had less genetic diversity than offshore dolphins. Further substructuring within the offshore stock was not detected. The level of genetic differentiation between the coastal and offshore dolphins is consistent with long‐term separation and reinforces recognizing them as separate stocks. These findings are particularly important for management of the smaller, less genetically diverse, coastal stock that is vulnerable to a variety of anthropogenic threats.     

RANGE CHARACTERISTICS OF PACIFIC COAST BOTTLENOSE DOLPHINS (TURSIOPS TRUNCATUS) IN THE SOUTHERN CALIFORNIA BIGHT

Boat-based photoidentification surveys of bottlenose dolphins (Tursiops truncatus) were conducted from 1982 to 1989 in three discrete coastal study areas within the Southern California Bight: (1) Santa Barbara, California; (2) Orange County, California; (3) Ensenada, Baja California, Mexico. A total of 207 recognizable dolphins were identified in these three “secondary” study areas. These individuals were compared to 404 dolphins identified from 1981 to 1989 in our “primary” study area, San Diego, California, to examine the coastal movement patterns of bottlenose dolphins within the Southern California Bight. A high proportion of dolphins photographed in Santa Barbara (88%), Orange County (92%), and Ensenada (88%) were also photographed in San Diego. Fifty-eight percent (n= 120) of these 207 dolphins exhibited back-and-forth movements between study areas, with no evidence of site fidelity to any particular region. Minimum range estimates were 50 and 470 km. Minimum travel-speed estimates were 11-47 km/d, and all dolphin schools sighted during the study were within 1 km of the shore. These data suggest that bottlenose dolphins within the Southern California Bight are highly mobile within a relatively narrow coastal zone. Home-range dimensions and movement patterns for many vettebrate species are influenced, in part, by variation in food resources. The unique range characteristics documented during this study may reflect the highly dynamic nature of this coastal ecosystem and the associated patchy distribution of food resources available to these bottlenose dolphins.     

Evidence for Distinct Coastal and Offshore Communities of Bottlenose Dolphins in the North East Atlantic

Bottlenose dolphin stock structure in the northeast Atlantic remains poorly understood. However, fine scale photo-id data have shown that populations can comprise multiple overlapping social communities. These social communities form structural elements of bottlenose dolphin (Tursiops truncatus) populations, reflecting specific ecological and behavioural adaptations to local habitats. We investigated the social structure of bottlenose dolphins in the waters of northwest Ireland and present evidence for distinct inshore and offshore social communities. Individuals of the inshore community had a coastal distribution restricted to waters within 3 km from shore. These animals exhibited a cohesive, fission-fusion social organisation, with repeated resightings within the research area, within a larger coastal home range. The offshore community comprised one or more distinct groups, found significantly further offshore (>4 km) than the inshore animals. In addition, dorsal fin scarring patterns differed significantly between inshore and offshore communities with individuals of the offshore community having more distinctly marked dorsal fins. Specifically, almost half of the individuals in the offshore community (48%) had characteristic stereotyped damage to the tip of the dorsal fin, rarely recorded in the inshore community (7%). We propose that this characteristic is likely due to interactions with pelagic fisheries. Social segregation and scarring differences found here indicate that the distinct communities are likely to be spatially and behaviourally segregated. Together with recent genetic evidence of distinct offshore and coastal population structures, this provides evidence for bottlenose dolphin inshore/offshore community differentiation in the northeast Atlantic. We recommend that social communities should be considered as fundamental units for the management and conservation of bottlenose dolphins and their habitat specialisations.     

Acid treatment effects on the stable isotopic signatures of fossils

Abstract: Prior to geochemical analyses, fossil bones and teeth are often extracted from any surrounding lithified sediments using chemical techniques such as immersion in acid. As stable isotope analysis becomes more commonplace in palaeoecological investigations, it is important to consider what effects these chemical preparation techniques may have on any subsequent isotopic data and to constrain these effects as quantitatively as possible. This study aims to elucidate these effects, as it is vital that variability in a data set should not be introduced as a result of protocols used during sample preparation; in addition, it defines the most effective and viable method of carbonate removal for processing bulk fossil samples without causing alteration of their stable isotopic signatures. Various strengths of two weak acids commonly used during palaeontological preparation were tested to evaluate their effects on the δ¹⁵N and δ¹³C_org isotopic signatures of the vertebrae of a large Eocene fossil fish. Changes in the isotopic values occurred over time regardless of which acid was used, each causing a variable response in both δ¹⁵N and δ¹³C_org isotopic values. Without careful monitoring of the acidification process in a controlled environment, any resulting data could therefore confound interpretation. Based on these experiments, it is recommended that 2 m acetic acid be used for the pretreatment of fossils prior to the acquisition of N and C isotope data where carbonate removal is necessary.     

Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (<Emphasis Type="Italic">Tursiops truncatus</Emphasis>) in the Gulf of Mexico

There is a need for biological information to support current stock designations of bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. The existence of many inshore, resident “communities” raises questions as to the relationship these dolphins may hold with dolphins inhabiting neighboring inshore and coastal areas. In this study, population subdivision was examined among four resident, inshore bottlenose dolphin stocks (Sarasota Bay, FL, Tampa Bay, FL, Charlotte Harbor, FL and Matagorda Bay, TX) and one coastal stock (1–12 km offshore) in the Gulf of Mexico. Evidence of significant population structure among all areas was found on the basis of both mitochondrial DNA (mtDNA) control region sequence data and nine nuclear microsatellite loci. Estimates of relatedness showed no population contained a significantly high number of related individuals, while separate AMOVAs for males and females indicated that both sexes exhibit a significant level of site philopatry. Results presented here provide the first genetic evidence of population subdivision between the coastal Gulf of Mexico and adjacent inshore areas along the central west coast of Florida. Such strong genetic subdivision is surprising given the short geographical distance between many of these areas and the lack of obvious geographic barriers to prevent gene flow. These findings support the current, separate identification of stocks for bottlenose dolphins inhabiting the eastern coastal and inshore areas of the Gulf of Mexico.