Long-Term Consequences of High Polychlorinated Biphenyl Exposure: Projected Decline of Delphinid Populations in a Hotspot for Chemical Pollution.

Rough-toothed dolphins, Steno bredanensis, are closely associated with coastal waters in the Southwestern Atlantic Ocean, increasing the exposure to multiple stressors, such as chemical pollution. Persistent organic pollutants (POPs) are known to affect the health of cetacean species. To comprehend the potential impacts of POPs on populations' viability, it is necessary to distinguish populations and predict their risk of long-term exposure. Blubbers of rough-toothed dolphins (n = 28) collected along the southeastern (SE) and southern (S) Brazilian coast were screened for polychlorinated biphenyls (PCBs) and pesticides in a gas chromatograph coupled to a mass spectrometer. Based on the contamination profile, a discriminant function analysis separated the rough-toothed dolphins into three ecological populations: two coastal and one offshore. POP concentrations were the highest reported for the species worldwide and highest among the delphinids in Brazilian waters, reaching 647.9 µg g-1 lw for PCBs. The SE population presented 212.9 ± 163.0, S population presented 101.0 ± 96.7, and OCS/S population presented 183.3 ± 85.3 µg g-1 lw (mean ± SD) of PCBs. The potential risk of effects triggered by elevated PCB concentrations was assessed in an individual-based model. A risk of severe decline in population size is projected for the three populations in the next 100 years, especially in SE Brazil, varying between 67 and 99%.

Combining isotopic analysis of bulk-skin and individual amino acids to investigate the trophic position and foraging areas of multiple cetacean species in the western South Atlantic.

We investigated the trophic structure and habitat use of ten cetacean species occurring in the oceanic waters of the western South Atlantic using naturally-occurring stable isotopes. We analysed δ15N in individual amino acids (AA) to estimate cetacean trophic position (TP) and to evaluate the spatial differences in baseline δ15N (source AAs). We adjusted cetacean bulk-skin δ13C and δ15N for the effect of trophic level using their estimated TPs, obtaining δ13CAdjusted and δ15NAdjusted, respectively. These values were applied to estimate the overlap in the niche areas of cetacean baseline sources. Our analyses showed spatial segregation between Steno bredanensis and the remaining odontocetes, and the high δ15N in this species reflects its occurrence in neritic waters of the southern region. The highest TPs were observed in Physeter macrocephalus, Stenella attenuata and Globicephala melas, while the lowest TPs were reported for S. longirostris, S. clymene and Orcinus orca. Overall, source AA-δ15N showed similar patterns as those of baseline-δ15N (zooplankton) and were higher in species sampled in the southernmost region of the study area (e.g., Delphinus delphis). Isotopic niche areas estimated using δ13CAdjusted and δ15NAdjusted suggested high overlap in foraging area between S. frontalis and Tursiops truncatus, with the latter occupying a higher TP. Our analyses of δ15N in AAs provide a unique insight into the trophic ecology, forage areas and spatial segregation in resource use among these cetacean populations. Additionally, our work provides AA-δ15N baseline for future studies on the trophic ecology and habitat use of marine organisms in the western South Atlantic.

Diverse groups of fungi are associated with plastics in the surface waters of the Western South Atlantic and the Antarctic Peninsula.

Marine plastic pollution has a range of negative impacts for biota and the colonization of plastics in the marine environment by microorganisms may have significant ecological impacts. However, data on epiplastic organisms, particularly fungi, is still lacking for many ocean regions. To evaluate plastic associated fungi and their geographic distribution, we characterised plastics sampled from surface waters of the western South Atlantic (WSA) and Antarctic Peninsula (AP), using DNA metabarcoding of three molecular markers (ITS2, 18S rRNA V4 and V9 regions). Numerous taxa from eight fungal phyla and a total of 64 orders were detected, including groups that had not yet been described associated with plastics. There was a varied phylogenetic assemblage of predominantly known saprotrophic taxa within the Ascomycota and Basidiomycota. We found a range of marine cosmopolitan genera present on plastics in both locations, i.e., Aspergillus, Cladosporium, Wallemia and a number of taxa unique to each region, as well as a high variation of taxa such as Chytridiomycota and Aphelidomycota between locations. Within these basal fungal groups we identified a number of phylogenetically novel taxa. This is the first description of fungi from the Plastisphere within the Southern Hemisphere, and highlights the need to further investigate the potential impacts of plastic associated fungi on other organisms and marine ecosystems.

Effects of acidification on the isotopic ratios of Neotropical otter tooth dentin.

RATIONALE: Stable carbon and nitrogen isotope ratios are widely used in ecological studies providing important information on the trophic ecology and habitat use of consumers. However, some factors may lead to isotopic variability, which makes difficult the interpretation of data, such as the presence of inorganic carbon in mineralized tissues. In order to remove the inorganic carbon, acidification is a commonly used treatment. METHODS: The effects of two methods of acidification were tested: (i) dentin acidification with 10% HCl using the 'drop-by-drop' technique, and (ii) dentin acidification in an 'HCl atmosphere', by exposing the dentin to vaporous 30% hydrochloric acid. Results were compared with untreated subsamples. The stable carbon and nitrogen ratios of untreated and acidified subsamples were measured using an elemental analyzer coupled to an isotope ratio mass spectrometer. RESULTS: The nitrogen isotopic ratios were statistically different between the two acidification treatments, but no significant changes in carbon isotopic ratios were found in acidified and untreated samples. CONCLUSIONS: The results indicated that acidification had no effect on carbon isotopic ratios of Neotropical otter tooth dentin, while introducing a source of error in nitrogen isotopic ratios. Therefore, we conclude that acidification is an unnecessary step for C and N stable isotope analysis.

Effects of acidification, lipid removal and mathematical normalization on carbon and nitrogen stable isotope compositions in beaked whale (Ziphiidae) bone.

RATIONALE: The analysis of stable isotopes in tissues such as teeth and bones has been used to study long-term trophic ecology and habitat use in marine mammals. However, carbon isotope ratios (δ(13) C values) can be altered by the presence of (12) C-rich lipids and carbonates. Lipid extraction and acidification are common treatments used to remove these compounds. The impact of lipids and carbonates on carbon and nitrogen isotope ratios (δ(15) N values), however, varies among tissues and/or species, requiring taxon-specific protocols to be developed. METHODS: The effects of lipid extraction and acidification and their interaction on carbon and nitrogen isotope values were studied for beaked whale (Ziphiidae) bone samples. δ(13) C and δ(15) N values were determined in quadruplicate samples: control, lipid-extracted, acidified and lipid-extracted followed by acidification. Samples were analyzed by means of elemental analysis isotope ratio mass spectrometry. Furthermore, the efficiency of five mathematical models developed for estimating lipid-normalized δ(13) C values from untreated δ(13) C values was tested. RESULTS: Significant increases in δ(13) C values were observed after lipid extraction. No significant changes in δ(13) C values were found in acidified samples. An interaction between both treatments was demonstrated for δ(13) C but not for δ(15) N values. No change was observed in δ(15) N values for lipid-extracted and/or acidified samples. Although all tested models presented good predictive power to estimate lipid-free δ(13) C values, linear models performed best. CONCLUSIONS: Given the observed changes in δ(13) C values after lipid extraction, we recommend a priori lipid extraction or a posteriori lipid normalization, through simple linear models, for beaked whale bones. Furthermore, acidification seems to be an unnecessary step before stable isotope analysis, at least for bone samples of ziphiids. Copyright © 2015 John Wiley & Sons, Ltd.

Anthropogenic debris in three sympatric seal species of the Western Antarctic Peninsula.

Litter pollution is a growing concern, including for Antarctica and the species that inhabit this ecosystem. In this study, we investigated the microplastic contamination in three seal species that inhabit the Western Antarctic Peninsula: crabeater (Lobodon carcinophaga), leopard (Hydrurga leptonyx) and Weddell (Leptonychotes weddellii) seals. Given the worldwide ubiquity of this type of contaminant, including the Southern Ocean, we hypothesized that the three seal species would present anthropogenic debris in their feces. We examined 29 scat samples of crabeater (n = 5), leopard (n = 13) and Weddell (n = 11) seals. The chemical composition of the items found were identified using micro-Raman and micro-FTIR spectroscopies. All the samples of the three species presented anthropic particles (frequency of occurrence - %FO - 100 %). Fibers were the predominant debris, but fragments and filaments were also present. Particles smaller than 5 mm (micro debris) were predominant in all the samples. Leopard seals ingested significantly larger micro-debris in comparison with the other seal species. The dominant color was black followed by blue and white. Micro-Raman and micro-FTIR Spectroscopies revealed the presence of different anthropogenic pigments such as reactive blue 238, Indigo 3600 and copper phthalocyanine (blue and green). Carbon black was also detected in the samples, as well as plastic polymers such as polystyrene, polyester and polyethylene terephthalate (PET), polyamide, polypropylene and polyurethane These results confirm the presence of anthropogenic contamination in Antarctic seals and highlight the need for actions to mitigate the effects and reduce the contribution of debris in the Antarctic ecosystem.

Potential biases in dietary interpretation derived from stable isotope analysis of small dolphin teeth.

We analyzed δ13C and δ15N values in different tooth portions (Growth Layer Groups, GLGs) of franciscanas, Pontoporia blainvillei, to investigate their effect on whole tooth (WT) isotopic values and the implications for dietary estimates. Tooth portions included the dentin deposited during the prenatal development (PND), the first year of life (GLG1) deposited during the nursing period and the central part of the tooth with no distinction amongst subsequent GLGs (Center). Isotopic mixing models estimating the contribution of PND, GLG1 and Center to WT showed that GLG1 has a strong effect on WT isotope values in juveniles, while Center only starts to affect WT isotopic values from age four. Isotopic mixing models estimating prey contribution to the diet of juveniles using WT vs Center tooth portions significantly differed in dietary outputs, demonstrating that GLG1 influence on WT isotope values affects dietary estimates in young franciscanas. As the small tooth size and narrowness of the last GLGs hinder the analysis of individual layers, we recommend excluding GLG1 in studies based on teeth isotope composition in franciscanas and caution when interpreting isotopic values from the WT of other small cetaceans.

An additional threat to populations predicted to collapse: Organobromine compounds of natural and anthropogenic sources in rough-toothed dolphins from the Southwestern Atlantic Ocean.

Organic contaminants with toxic effects, like the conventional brominated flame retardants (BFRs) and BFRs of emergent concern, and their synergistic effects with other micropollutants, can be an additional threat to delphinids. Rough-toothed dolphins (Steno bredanensis) populations strongly associated with coastal environments already face a potential risk of decline due to high exposure to organochlorine pollutants. Moreover, natural organobromine compounds are important indicators of the environment's health. Polybrominated diphenyl ethers (PBDEs), pentabromoethylbenzene (PBEB), hexabromobenzene (HBB) and the methoxylated PBDEs (MeO-BDEs) were determined in the blubber of rough-toothed dolphins from three ecological populations from the Southwestern Atlantic Ocean (Southeastern, Southern and Outer Continental Shelf/Southern populations, SE, S, and OCS/S, respectively). The profile was dominated by the naturally produced MeO-BDEs (mainly 2'-MeO-BDE 68 and 6-MeO-BDE 47), followed by the anthropogenic BFRs PBDEs (mainly BDE 47). Median ΣMeO-BDE concentrations varied between 705.4 and 3346.0 ng g-1 lw among populations and ΣPBDE from 89.4 until 538.0 ng g-1 lw. Concentrations of anthropogenic organobromine compounds (ΣPBDE, BDE 99 and BDE 100) were higher in SE population than in OCS/S, indicating a coast - ocean gradient of contamination. Negative correlations were found between the concentration of the natural compounds and age, suggesting their metabolization and/or biodilution and maternal transference. Conversely, positive correlations were found between the concentrations of BDE 153 and BDE 154 and age, indicating low biotransformation capability of these heavy congeners. The levels of PBDEs found are concerning, particularly for SE population, because they are similar to concentrations known for the onset of endocrine disruption in other marine mammals and may be an additional threat to a population in a hotspot for chemical pollution.

The deep dive of organohalogen compounds: Bioaccumulation in the top predators of mesopelagic trophic webs, pygmy and dwarf sperm whales, from the Southwestern Atlantic ocean.

Kogia sima and Kogia breviceps are apex predators of mesopelagic trophic webs being far from most anthropogenic threats. However, chemical pollutants and naturally synthesized compounds may travel long distances. This study aimed to use kogiid whales as sentinels of mesopelagic trophic webs in the Southwestern Atlantic Ocean. Persistent organic pollutants (POPs), e.g., polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT) and metabolites, mirex, hexachlorobenzene (HCB), polybrominated diphenylethers (PBDEs), pentabromoethylbenzene (PBEB) and hexabromobenzene (HBB), and the naturally produced methoxylated BDE (MeO-BDEs) were determined in the blubber of 16 K. sima and 15 K. breviceps. Among the organochlorine compounds, DDTs were the main group found in K. sima and in K. breviceps (1636.6 and 3983.3 ng g-1 lw, respective medians), followed by PCBs (425.9 and 956.1 ng g-1 lw, respectively), mirex (184.1 and 375.6 ng g-1 lw, respectively), and HCB (132.4 and 340.3 ng g-1 lw, respectively). As for the organobromine, the natural MeO-BDEs were predominant (1676.7 and 501.6 ng g-1 lw, respectively), followed by PBDEs (13.6 and 10.3 ng g-1 lw, respectively) and PBEB (2.2 and 2.9 ng g-1 lw, respectively). In general, POPs concentration was higher in K. breviceps than in K. sima. Conversely, MeO-BDEs concentration was higher in K. sima than in K. breviceps. Differences in concentrations in these sympatric odontocetes were attributed to distinct species, sampling sites, and biological parameters and suggest some level of niche segregation. It is noteworthy the long-range reach and bioaccumulation of these synthetic compounds in an unexplored habitat, that present an increasing economic interest.

Long-Term Seasonal and Interannual Patterns of Marine Mammal Strandings in Subtropical Western South Atlantic.

Understanding temporal patterns of marine mammal occurrence is useful for establishing conservation strategies. We used a 38 yr-long dataset spanning 1976 to 2013 to describe temporal patterns and trends in marine mammal strandings along a subtropical stretch of the east coast of South America. This region is influenced by a transitional zone between tropical and temperate waters and is considered an important fishing ground off Brazil. Generalized Additive Models were used to evaluate the temporal stranding patterns of the most frequently stranded species. Forty species were documented in 12,540 stranding events. Franciscana (n = 4,574), South American fur seal, (n = 3,419), South American sea lion (n = 2,049), bottlenose dolphins (n = 293) and subantarctic fur seal (n = 219) were the most frequently stranded marine mammals. The seasonality of strandings of franciscana and bottlenose dolphin coincided with periods of higher fishing effort and strandings of South American and subantarctic fur seals with post-reproductive dispersal. For South American sea lion the seasonality of strandings is associated with both fishing effort and post-reproductive dispersal. Some clear seasonal patterns were associated with occurrence of cold- (e.g. subantarctic fur seal) and warm-water (e.g. rough-toothed dolphin) species in winter and summer, respectively. Inter-annual increases in stranding rate were observed for franciscana and South American fur seal and these are likely related to increased fishing effort and population growth, respectively. For subantarctic fur seal the stranding rate showed a slight decline while for bottlenose dolphin it remained steady. No significant year to year variation in stranding rate was observed for South American sea lion. The slight decrease in frequency of temperate/polar marine mammals and the increased occurrence of subtropical/tropical species since the late 1990s might be associated with environmental changes linked to climate change. This long-term study indicates that temporal stranding patterns of marine mammals might be explained by either fishing-related or environmental factors.

High accumulation of PCDD, PCDF, and PCB congeners in marine mammals from Brazil: a serious PCB problem.

Blubber samples from three delphinid species (false killer whale, Guiana and rough-toothed dolphin), as well as liver samples from franciscana dolphins were analyzed for dioxins and related compounds (DRCs). Samples were collected from 35 cetaceans stranded or incidentally captured in a highly industrialized and urbanized area (Southeast and Southern Brazilian regions). Dioxin-like PCBs accounted for over 83% of the total TEQ for all cetaceans. Non-ortho coplanar PCBs, for franciscanas (82%), and mono-ortho PCBs (up to 80%), for delphinids, constituted the groups of highest contribution to total TEQ. Regarding franciscana dolphins, significant negative correlations were found between total length (TL) and three variables, ΣTEQ-DRCs, ΣTEQ-PCDF and ΣTEQ non-ortho PCB. An increasing efficiency of the detoxifying activity with the growth of the animal may be a plausible explanation for these findings. This hypothesis is reinforced by the significant negative correlation found between TL and PCB126/PCB169 concentration ratio. DRC concentrations (ng/g lipids) varied from 36 to 3006, for franciscana dolphins, as well as from 356 to 30,776, for delphinids. The sum of dioxin-like and indicator PCBs varied from 34,662 to 279,407 ng/g lipids, for Guiana dolphins from Rio de Janeiro state, which are among the highest PCB concentrations ever reported for cetaceans. The high concentrations found in our study raise concern not only on the conservation of Brazilian coastal cetaceans, but also on the possibility of human health problem due to consumption of fish from Brazilian estuaries.