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1.  Harbour Porpoises Phocoena phocoena in the Eastern Scheldt: A Resident Stock or Trapped by a Storm Surge Barrier? 
PLoS ONE  2013;8(3):e56932.
Coastal protection measures are planned and executed worldwide to combat the effects of global warming and climate change, in particular the acceleration of sea level rise, higher storm surge flooding and extensive coastal inundation. The extent to which these defensive measures may impact coastal and estuarine ecosystems is still poorly understood. Since the building of a storm surge barrier, movement of harbour porpoises Phocoena phocoena in and out of the Eastern Scheldt tidal bay (SW-Netherlands) may be limited. To measure residency, porpoises stranded along the Dutch North Sea coast between 2006 and 2008 were sampled for muscle (n = 102) and bone tissue (n = 118), of which 9 muscle (8.8%) and 12 bone samples (10.2%) were collected from animals stranded within the Eastern Scheldt. Stable carbon (δ13C) was analysed to get insight into the habitat use and residency of porpoises in the Eastern Scheldt. Our data showed significantly higher δ13C values in the muscle of porpoises stranded within the Eastern Scheldt (µ = −17.7‰, SD = 0.4‰) compared to animals stranded along the Dutch coast (µ = −18.3‰, SD = 0.5‰). This suggests that most porpoises stranded in the Eastern Scheldt foraged there for a longer period. The distinct δ13C signature of animals from the Eastern Scheldt was not observed in bone tissue, suggesting a relatively recent shift in habitat use rather than life-long residency of porpoises within the Eastern Scheldt. The high number of strandings within the Eastern Scheldt suggests a higher mortality rate compared to the Dutch coastal zone. Our study indicates that along with other changes in the physical environment, the storm surge barrier may play an important role in determining the residency of porpoises in the Eastern Scheldt, and that the area might act as an ecological trap for porpoises entering it.
doi:10.1371/journal.pone.0056932
PMCID: PMC3590242  PMID: 23483892
2.  Bartonella henselae in Porpoise Blood 
Emerging Infectious Diseases  2005;11(12):1894-1898.
DNA in porpoises suggests an emerging infectious disease in marine mammals.
We report detection of Bartonella henselae DNA in blood samples from 2 harbor porpoises (Phocoena phocoena). By using real-time polymerase chain reaction, we directly amplified Bartonella species DNA from blood of a harbor porpoise stranded along the northern North Carolina coast and from a preenrichment blood culture from a second harbor porpoise. The second porpoise was captured out of habitat (in a low-salinity canal along the northern North Carolina coast) and relocated back into the ocean. Subsequently, DNA was amplified by conventional polymerase chain reaction for DNA sequencing. The 16S–23S intergenic transcribed spacer region obtained from each porpoise was 99.8% similar to that of B. henselae strain San Antonio 2 (SA2), whereas both heme-binding phage-associated pap31 gene sequences were 100% homologous to that of B. henselae SA2. Currently, the geographic distribution, mode of transmission, reservoir potential, and pathogenicity of bloodborne Bartonella species in porpoises have not been determined.
doi:10.3201/eid1112.050969
PMCID: PMC3367652  PMID: 16485476
Bartonella; cetacean; porpoise; emerging; stranded; research
3.  The Stranding Anomaly as Population Indicator: The Case of Harbour Porpoise Phocoena phocoena in North-Western Europe 
PLoS ONE  2013;8(4):e62180.
Ecological indicators for monitoring strategies are expected to combine three major characteristics: ecological significance, statistical credibility, and cost-effectiveness. Strategies based on stranding networks rank highly in cost-effectiveness, but their ecological significance and statistical credibility are disputed. Our present goal is to improve the value of stranding data as population indicator as part of monitoring strategies by constructing the spatial and temporal null hypothesis for strandings. The null hypothesis is defined as: small cetacean distribution and mortality are uniform in space and constant in time. We used a drift model to map stranding probabilities and predict stranding patterns of cetacean carcasses under H0 across the North Sea, the Channel and the Bay of Biscay, for the period 1990–2009. As the most common cetacean occurring in this area, we chose the harbour porpoise Phocoena phocoena for our modelling. The difference between these strandings expected under H0 and observed strandings is defined as the stranding anomaly. It constituted the stranding data series corrected for drift conditions. Seasonal decomposition of stranding anomaly suggested that drift conditions did not explain observed seasonal variations of porpoise strandings. Long-term stranding anomalies increased first in the southern North Sea, the Channel and Bay of Biscay coasts, and finally the eastern North Sea. The hypothesis of changes in porpoise distribution was consistent with local visual surveys, mostly SCANS surveys (1994 and 2005). This new indicator could be applied to cetacean populations across the world and more widely to marine megafauna.
doi:10.1371/journal.pone.0062180
PMCID: PMC3632559  PMID: 23614031
4.  A European Melting Pot of Harbour Porpoise in the French Atlantic Coasts Inferred from Mitochondrial and Nuclear Data 
PLoS ONE  2012;7(9):e44425.
Field surveys have reported a global shift in harbour porpoise distribution in European waters during the last 15 years, including a return to the Atlantic coasts of France. In this study, we analyzed genetic polymorphisms at a fragment of the mitochondrial control region (mtDNA CR) and 7 nuclear microsatellite loci, for 52 animals stranded and by-caught between 2000 and 2010 along the Atlantic coasts of France. The analysis of nuclear and mitochondrial loci provided contrasting results. The mtDNA revealed two genetically distinct groups, one closely related to the Iberian and African harbour porpoises, and the second related to individuals from the more northern waters of Europe. In contrast, nuclear polymorphisms did not display such a distinction. Nuclear markers suggested that harbour porpoises behaved as a randomly mating population along the Atlantic coasts of France. The difference between the two kinds of markers can be explained by differences in their mode of inheritance, the mtDNA being maternally inherited in contrast to nuclear loci that are bi-parentally inherited. Our results provide evidence that a major proportion of the animals we sampled are admixed individuals from the two genetically distinct populations previously identified along the Iberian coasts and in the North East Atlantic. The French Atlantic coasts are clearly the place where these two previously separated populations of harbour porpoises are now admixing. The present shifts in distribution of harbour porpoises along this coast is likely caused by habitat changes that will need to be further studied.
doi:10.1371/journal.pone.0044425
PMCID: PMC3440431  PMID: 22984507
5.  Linking sandeel consumption and the likelihood of starvation in harbour porpoises in the Scottish North Sea: could climate change mean more starving porpoises? 
Biology Letters  2007;3(2):185-188.
Sandeels are known to be negatively affected by climate change in a number of ways. This study investigated whether these changes are affecting the harbour porpoise (Phocoena phocoena), a species which consumes sandeels. Porpoise diet was examined in spring (March–May), a critical time of year for survival when sandeels are important prey, from 1993 to 2001 to provide baseline information on the proportion of sandeels consumed. When data from spring 2002 and 2003 were compared to these baseline data, the diet was found to be substantially different, with a significant and substantially smaller proportion of sandeels being consumed in March and May. There were also differences in the number of porpoises starving between the two time periods (33% in spring 2002 and 2003 died of starvation, but only 5% in the baseline period). This suggests that a lower proportion of sandeels in the diet of porpoises in spring increases the likelihood of starvation. Therefore, we suggest that the negative effects of climate change on sandeel availability may have serious negative effects on harbour porpoise populations in the North Sea by increasing the likelihood of starvation in spring.
doi:10.1098/rsbl.2006.0588
PMCID: PMC2375924  PMID: 17251125
harbour porpoise; sandeels; climate change
6.  Genetic and historic evidence for climate-driven population fragmentation in a top cetacean predator: the harbour porpoises in European water 
Recent climate change has triggered profound reorganization in northeast Atlantic ecosystems, with substantial impact on the distribution of marine assemblages from plankton to fishes. However, assessing the repercussions on apex marine predators remains a challenging issue, especially for pelagic species. In this study, we use Bayesian coalescent modelling of microsatellite variation to track the population demographic history of one of the smallest temperate cetaceans, the harbour porpoise (Phocoena phocoena) in European waters. Combining genetic inferences with palaeo-oceanographic and historical records provides strong evidence that populations of harbour porpoises have responded markedly to the recent climate-driven reorganization in the eastern North Atlantic food web. This response includes the isolation of porpoises in Iberian waters from those further north only approximately 300 years ago with a predominant northward migration, contemporaneous with the warming trend underway since the ‘Little Ice Age’ period and with the ongoing retreat of cold-water fishes from the Bay of Biscay. The extinction or exodus of harbour porpoises from the Mediterranean Sea (leaving an isolated relict population in the Black Sea) has lacked a coherent explanation. The present results suggest that the fragmentation of harbour distribution range in the Mediterranean Sea was triggered during the warm ‘Mid-Holocene Optimum’ period (approx. 5000 years ago), by the end of the post-glacial nutrient-rich ‘Sapropel’ conditions that prevailed before that time.
doi:10.1098/rspb.2010.0412
PMCID: PMC2981983  PMID: 20444724
cetacean; climate change; habitat fragmentation; population genetics; coalescence
7.  Harbour porpoises respond to climate change 
Ecology and Evolution  2011;1(4):579-585.
The effects of climate change on marine ecosystems and in particular on marine top predators are difficult to assess due to, among other things, spatial variability, and lack of clear delineation of marine habitats. The banks of West Greenland are located in a climate sensitive area and are likely to elicit pronounced responses to oceanographic changes in the North Atlantic. The recent increase in sea temperatures on the banks of West Greenland has had cascading effects on sea ice coverage, residency of top predators, and abundance of important prey species like Atlantic cod (Gadus morhua). Here, we report on the response of one of the top predators in West Greenland; the harbour porpoise (Phocoena phocoena). The porpoises depend on locating high densities of prey species with high nutritive value and they have apparently responded to the general warming on the banks of West Greenland by longer residence times, increased consumption of Atlantic cod resulting in improved body condition in the form of larger fat deposits in blubber, compared to the situation during a cold period in the 1990s. This is one of the few examples of a measurable effect of climate change on a marine mammal population.
doi:10.1002/ece3.51
PMCID: PMC3287339  PMID: 22393524
Climate change; harbour porpoise; west greenland; body condition; Atlantic cod
8.  Zn, Cu, Cd and Hg binding to metallothioneins in harbour porpoises Phocoena phocoena from the southern North Sea 
BMC Ecology  2006;6:2.
Background
Harbour porpoises Phocoena phocoena from the southern North Sea are known to display high levels of Zn and Hg in their tissues linked to their nutritional status (emaciation). The question arises regarding a potential role of metallothioneins (MTs) with regard to these high metal levels. In the present study, metallothionein detection and associated Zn, Cd, Cu and Hg concentrations were investigated in the liver and kidney of 14 harbour porpoises collected along the Belgian coast.
Results
Metallothioneins seemed to play a key role in essential metal homeostasis, as they were shown to bind 50% of the total hepatic Zn and 36% of the total hepatic Cu concentrations. Renal MTs also participated in Cd detoxification, as they were shown to bind 56% of the total renal Cd. Hg was mainly found in the insoluble fraction of both liver and kidney. Concomitant increases in total Zn concentration and Zn bound to MTs were observed in the liver, whereas Zn concentration bound to high molecular weight proteins remained constant. Cu, Zn and Cd were accumulated preferentially in the MT fraction and their content in this fraction increased with the amount in the hepatocytosol.
Conclusion
MTs have a key role in Zn and Cu homeostasis in harbour porpoises. We demonstrated that increasing hepatic Zn concentration led to an increase in Zn linked to MTs, suggesting that these small proteins take over the Zn overload linked to the poor body condition of debilitated harbour porpoises.
doi:10.1186/1472-6785-6-2
PMCID: PMC1434725  PMID: 16464247
9.  Exposing the grey seal as a major predator of harbour porpoises 
Harbour porpoises (Phocoena phocoena) stranding in large numbers around the southern North Sea with fatal, sharp-edged mutilations have spurred controversy among scientists, the fishing industry and conservationists, whose views about the likely cause differ. The recent detection of grey seal (Halichoerus grypus) DNA in bite marks on three mutilated harbour porpoises, as well as direct observations of grey seal attacks on porpoises, have identified this seal species as a probable cause. Bite mark characteristics were assessed in a retrospective analysis of photographs of dead harbour porpoises that stranded between 2003 and 2013 (n = 1081) on the Dutch coastline. There were 271 animals that were sufficiently fresh to allow macroscopic assessment of grey seal-associated wounds with certainty. In 25% of these, bite and claw marks were identified that were consistent with the marks found on animals that had tested positive for grey seal DNA. Affected animals were mostly healthy juveniles that had a thick blubber layer and had recently fed. We conclude that the majority of the mutilated harbour porpoises were victims of grey seal attacks and that predation by this species is one of the main causes of death in harbour porpoises in The Netherlands. We provide a decision tree that will help in the identification of future cases of grey seal predation on porpoises.
doi:10.1098/rspb.2014.2429
PMCID: PMC4262184  PMID: 25429021
marine mammals; mutilation; predation; DNA; bite mark; decision tree
10.  Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters 
BMC Biology  2007;5:30.
Background
Understanding the role of seascape in shaping genetic and demographic population structure is highly challenging for marine pelagic species such as cetaceans for which there is generally little evidence of what could effectively restrict their dispersal. In the present work, we applied a combination of recent individual-based landscape genetic approaches to investigate the population genetic structure of a highly mobile extensive range cetacean, the harbour porpoise in the eastern North Atlantic, with regards to oceanographic characteristics that could constrain its dispersal.
Results
Analyses of 10 microsatellite loci for 752 individuals revealed that most of the sampled range in the eastern North Atlantic behaves as a 'continuous' population that widely extends over thousands of kilometres with significant isolation by distance (IBD). However, strong barriers to gene flow were detected in the south-eastern part of the range. These barriers coincided with profound changes in environmental characteristics and isolated, on a relatively small scale, porpoises from Iberian waters and on a larger scale porpoises from the Black Sea.
Conclusion
The presence of these barriers to gene flow that coincide with profound changes in oceanographic features, together with the spatial variation in IBD strength, provide for the first time strong evidence that physical processes have a major impact on the demographic and genetic structure of a cetacean. This genetic pattern further suggests habitat-related fragmentation of the porpoise range that is likely to intensify with predicted surface ocean warming.
doi:10.1186/1741-7007-5-30
PMCID: PMC1971045  PMID: 17651495
11.  Estimating the spatial position of marine mammals based on digital camera recordings 
Ecology and Evolution  2015;5(3):578-589.
Estimating the spatial position of organisms is essential to quantify interactions between the organism and the characteristics of its surroundings, for example, predator–prey interactions, habitat selection, and social associations. Because marine mammals spend most of their time under water and may appear at the surface only briefly, determining their exact geographic location can be challenging. Here, we developed a photogrammetric method to accurately estimate the spatial position of marine mammals or birds at the sea surface. Digital recordings containing landscape features with known geographic coordinates can be used to estimate the distance and bearing of each sighting relative to the observation point. The method can correct for frame rotation, estimates pixel size based on the reference points, and can be applied to scenarios with and without a visible horizon. A set of R functions was written to process the images and obtain accurate geographic coordinates for each sighting. The method is applied to estimate the spatiotemporal fine-scale distribution of harbour porpoises in a tidal inlet. Video recordings of harbour porpoises were made from land, using a standard digital single-lens reflex (DSLR) camera, positioned at a height of 9.59 m above mean sea level. Porpoises were detected up to a distance of ∽3136 m (mean 596 m), with a mean location error of 12 m. The method presented here allows for multiple detections of different individuals within a single video frame and for tracking movements of individuals based on repeated sightings. In comparison with traditional methods, this method only requires a digital camera to provide accurate location estimates. It especially has great potential in regions with ample data on local (a)biotic conditions, to help resolve functional mechanisms underlying habitat selection and other behaviors in marine mammals in coastal areas.
doi:10.1002/ece3.1353
PMCID: PMC4328763
Distance; fine-scale distribution patterns; harbour porpoise; marine mammal; photogrammetric; theodolite; tide; video camera
12.  No Serological Evidence that Harbour Porpoises Are Additional Hosts of Influenza B Viruses 
PLoS ONE  2014;9(2):e89058.
Influenza A and B viruses circulate among humans causing epidemics almost annually. While various hosts for influenza A viruses exist, influenza B viruses have been detected only in humans and seals. However, recurrent infections of seals in Dutch coastal waters with influenza B viruses that are antigenetically distinct from influenza B viruses circulating among humans suggest that influenza B viruses have been introduced into this seal population by another, non-human, host. Harbour porpoises (Phocoena phocoena) are sympatric with seals in these waters and are also occasionally in close contact with humans after stranding and subsequent rehabilitation. In addition, virus attachment studies demonstrated that influenza B viruses can bind to cells of the respiratory tract of these animals. Therefore, we hypothesized that harbour porpoises might be a reservoir of influenza B viruses. In the present study, an unique set of serum samples from 79 harbour porpoises, stranded alive on the Dutch coast between 2003 and 2013, was tested for the presence of antibodies against influenza B viruses by use of the hemagglutination inhibition test and for antibodies against influenza A viruses by use of a competitive influenza A nucleoprotein ELISA. No antibodies were detected against either virus, suggesting that influenza A and B virus infections of harbour porpoises in Dutch coastal waters are not common, which was supported by statistical analysis of the dataset.
doi:10.1371/journal.pone.0089058
PMCID: PMC3923852  PMID: 24551217
13.  Population structure of harbour porpoises Phocoena phocoena in the seas around the UK and adjacent waters. 
The population structure of harbour porpoises from British and adjacent waters was studied by examining variability in a 200 bp (base pair) section of the control region of mitochondrial DNA (mtDNA) extracted from 327 animals. This region contained 20 variable sites giving rise to 24 different haplotypes. Mean nucleotide diversity between all pairs of haplotypes was 0.81% (range 0-4%). The most common haplotype occurred in 63% of the samples and was recorded in all geographical areas; several other haplotypes were present in two or more of the sampling locations. This suggests considerable historical interconnections among populations, probably through gene flow. However, there were significant differences (p < 0.05) as determined by AMOVA (Analysis of Molecular Variance, Excoffier et al. 1992), between porpoises from the northern and southern North Sea, and between the northern North Sea and the Celtic/Irish Sea. The differences were predominantly due to variation among females. This sex-related difference in population genetic structure suggests that males disperse more than females. This has important consequences for evaluating the consequences of incidental catches of porpoises by fisheries in these seas since there may be a greater impact on local populations than is implied by simple calculations of mortality.
PMCID: PMC1688231  PMID: 9061964
14.  The Influence of Topographic and Dynamic Cyclic Variables on the Distribution of Small Cetaceans in a Shallow Coastal System 
PLoS ONE  2014;9(1):e86331.
The influence of topographic and temporal variables on cetacean distribution at a fine-scale is still poorly understood. To study the spatial and temporal distribution of harbour porpoise Phocoena phocoena and the poorly known Risso’s dolphin Grampus griseus we carried out land-based observations from Bardsey Island (Wales, UK) in summer (2001–2007). Using Kernel analysis and Generalized Additive Models it was shown that porpoises and Risso’s appeared to be linked to topographic and dynamic cyclic variables with both species using different core areas (dolphins to the West and porpoises to the East off Bardsey). Depth, slope and aspect and a low variation in current speed (for Risso’s) were important in explaining the patchy distributions for both species. The prime temporal conditions in these shallow coastal systems were related to the tidal cycle (Low Water Slack and the flood phase), lunar cycle (a few days following the neap tidal phase), diel cycle (afternoons) and seasonal cycle (peaking in August) but differed between species on a temporary but predictable basis. The measure of tidal stratification was shown to be important. Coastal waters generally show a stronger stratification particularly during neap tides upon which the phytoplankton biomass at the surface rises reaching its maximum about 2–3 days after neap tide. It appeared that porpoises occurred in those areas where stratification is maximised and Risso’s preferred more mixed waters. This fine-scale study provided a temporal insight into spatial distribution of two species that single studies conducted over broader scales (tens or hundreds of kilometers) do not achieve. Understanding which topographic and cyclic variables drive the patchy distribution of porpoises and Risso’s in a Headland/Island system may form the initial basis for identifying potentially critical habitats for these species.
doi:10.1371/journal.pone.0086331
PMCID: PMC3899228  PMID: 24466031
15.  Leatherback Turtle Movements, Dive Behavior, and Habitat Characteristics in Ecoregions of the Northwest Atlantic Ocean 
PLoS ONE  2014;9(3):e91726.
Leatherback sea turtles, Dermochelys coriacea, are highly migratory predators that feed exclusively on gelatinous zooplankton, thus playing a unique role in coastal and pelagic food webs. From 2007 to 2010, we used satellite telemetry to monitor the movements and dive behavior of nine adult and eleven subadult leatherbacks captured on the Northeast USA shelf and tracked throughout the Northwest Atlantic. Leatherback movements and environmental associations varied by oceanographic region, with slow, sinuous, area-restricted search behavior and shorter, shallower dives occurring in cool (median sea surface temperature: 18.4°C), productive (median chlorophyll a: 0.80 mg m−3), shallow (median bathymetry: 57 m) shelf habitat with strong sea surface temperature gradients (median SST gradient: 0.23°C km−1) at temperate latitudes. Leatherbacks were highly aggregated in temperate shelf and slope waters during summer, early fall, and late spring and more widely dispersed in subtropical and tropical oceanic and neritic habitat during late fall, winter and early spring. We investigated the relationship of ecoregion, satellite-derived surface chlorophyll, satellite-derived sea surface temperature, SST gradient, chlorophyll gradient and bathymetry with leatherback search behavior using generalized linear mixed-effects models. The most well supported model showed that differences in leatherback search behavior were best explained by ecoregion and regional differences in bathymetry and SST. Within the Northwest Atlantic Shelves region, leatherbacks increased path sinuosity (i.e., looping movements) with increasing SST, but this relationship reversed within the Gulf Stream region. Leatherbacks increased path sinuosity with decreasing water depth in temperate and tropical shelf habitats. This relationship is consistent with increasing epipelagic gelatinous zooplankton biomass with decreasing water depth, and bathymetry may be a key feature in identifying leatherback foraging habitat in neritic regions. High-use habitat for leatherbacks in our study occurred in coastal waters of the North American eastern seaboard and eastern Caribbean, putting turtles at heightened risk from land- and ocean-based human activity.
doi:10.1371/journal.pone.0091726
PMCID: PMC3960146  PMID: 24646920
16.  The Diel Rhythms of Biosonar Behavior in the Yangtze Finless Porpoise (Neophocaena asiaeorientalis asiaeorientalis) in the Port of the Yangtze River: The Correlation between Prey Availability and Boat Traffic 
PLoS ONE  2014;9(5):e97907.
Information on the habitat use of the critically endangered Yangtze finless porpoise (Neophocaena asiaeorientalis asiaeorientalis) is critical for its conservation. The diel biosonar behavior of the porpoise in the port areas of the Yangtze River was examined along with simultaneous observations of fish density and boat traffic. Biosonar pulses from the porpoises were detected for 1233 min (5.77%) over a 21,380 min duration of effective observations. In total, 190 (5.63%) buzzes (an indication of prey capture attempts) were recorded among the 3372 identified click trains. Of the 168 echolocation encounters (bouts of click trains less than eight min apart), 150 (89.3%) involved single animals, indicating that solitary porpoises were frequently present and feeding in the port areas. Significant diel patterns were evident involving the biosonar behavior of the porpoises (including click trains and buzzes), fish density and boat traffic. The frequencies of the click trains and buzzes were significantly lower during the day than in the evening and at night, which suggests that porpoises in this region are primarily engaged in crepuscular and nocturnal foraging. The lack of a significant diel pattern in the echolocation encounters indicates the importance of the port in porpoise conservation. A forced feeding schedule may be associated with the lack of a significant correlation between porpoise acoustics and boat traffic. Overall, prey availability appears to be the primary factor that attracts porpoises. Additionally, porpoises tend to migrate or remain downstream in the morning and migrate or remain upstream in the evening, most likely to follow their prey. The findings of this study can be used to improve the conservation of the Yangtze finless porpoise.
doi:10.1371/journal.pone.0097907
PMCID: PMC4019666  PMID: 24823945
17.  Mass-dependent predation risk and lethal dolphin–porpoise interactions 
In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin ‘predation’ occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation–predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.
doi:10.1098/rspb.2007.0786
PMCID: PMC2275888  PMID: 17698485
energy reserves; starvation risk; starvation–predation risk trade-off; Phocoena phocoena; Tursiops truncatus
18.  Evaluation of immune and stress status in harbour porpoises (Phocoena phocoena): can hormones and mRNA expression levels serve as indicators to assess stress? 
Background
The harbour porpoise is exposed to increasing pressure caused by anthropogenic activities in its marine environment. Numerous offshore wind farms are planned or under construction in the North and Baltic Seas, which will increase underwater noise during both construction and operation. A better understanding of how anthropogenic impacts affect the behaviour, health, endocrinology, immunology and physiology of the animals is thus needed. The present study compares levels of stress hormones and mRNA expression of cytokines and acute-phase proteins in blood samples of harbour porpoises exposed to different levels of stress during handling, in rehabilitation or permanent human care.
Free-ranging harbour porpoises, incidentally caught in pound nets in Denmark, were compared to harbour porpoises in rehabilitation at SOS Dolfijn in Harderwijk, the Netherlands, and individuals permanently kept in human care in the Dolfinarium Harderwijk and Fjord & Belt Kerteminde, Denmark. Blood samples were investigated for catecholamines, adrenaline, noradrenaline and dopamine, as well as for adrenocorticotropic hormone (ACTH), cortisol, metanephrine and normetanephrine. mRNA expression levels of relevant cell mediators (cytokines IL-10 and TNFα, acute-phase proteins haptoglobin and C-reactive protein and the heat shock protein HSP70) were measured using real-time PCR.
Results
Biomarker expression levels varied between free-ranging animals and porpoises in human care. Hormone and cytokine ranges showed correlations to each other and to the health status of investigated harbour porpoises. Hormone concentrations were higher in free-ranging harbour porpoises than in animals in human care. Adrenaline can be used as a parameter for the initial reaction to acute stress situations; noradrenaline, dopamine, ACTH and cortisol are more likely indicators for the following minutes of acute stress. There is evidence for different correlations between production of normetanephrine, metanephrine, cortisol and the expression of IL-10, HSP70 and haptoglobin.
Conclusions
The expression patterns of the selected molecular biomarkers of the immune system are promising to reflect the health and immune status of the harbour porpoise under different levels of stress.
doi:10.1186/1746-6148-9-145
PMCID: PMC3734172  PMID: 23866055
Harbour porpoise; Stress hormones; Cytokines; Anthropogenic impact; Offshore wind farms; Underwater noise
19.  Isotope Analysis Reveals Foraging Area Dichotomy for Atlantic Leatherback Turtles 
PLoS ONE  2008;3(3):e1845.
Background
The leatherback turtle (Dermochelys coriacea) has undergone a dramatic decline over the last 25 years, and this is believed to be primarily the result of mortality associated with fisheries bycatch followed by egg and nesting female harvest. Atlantic leatherback turtles undertake long migrations across ocean basins from subtropical and tropical nesting beaches to productive frontal areas. Migration between two nesting seasons can last 2 or 3 years, a time period termed the remigration interval (RI). Recent satellite transmitter data revealed that Atlantic leatherbacks follow two major dispersion patterns after nesting season, through the North Gulf Stream area or more eastward across the North Equatorial Current. However, information on the whole RI is lacking, precluding the accurate identification of feeding areas where conservation measures may need to be applied.
Methodology/Principal Findings
Using stable isotopes as dietary tracers we determined the characteristics of feeding grounds of leatherback females nesting in French Guiana. During migration, 3-year RI females differed from 2-year RI females in their isotope values, implying differences in their choice of feeding habitats (offshore vs. more coastal) and foraging latitude (North Atlantic vs. West African coasts, respectively). Egg-yolk and blood isotope values are correlated in nesting females, indicating that egg analysis is a useful tool for assessing isotope values in these turtles, including adults when not available.
Conclusions/Significance
Our results complement previous data on turtle movements during the first year following the nesting season, integrating the diet consumed during the year before nesting. We suggest that the French Guiana leatherback population segregates into two distinct isotopic groupings, and highlight the urgent need to determine the feeding habitats of the turtle in the Atlantic in order to protect this species from incidental take by commercial fisheries. Our results also emphasize the use of eggs, a less-invasive sampling material than blood, to assess isotopic data and feeding habits for adult female leatherbacks.
doi:10.1371/journal.pone.0001845
PMCID: PMC2267998  PMID: 18365003
20.  The use of DNA barcoding to monitor the marine mammal biodiversity along the French Atlantic coast 
ZooKeys  2013;5-24.
In the last ten years, 14 species of cetaceans and five species of pinnipeds stranded along the Atlantic coast of Brittany in the North West of France. All species included, an average of 150 animals strand each year in this area. Based on reports from the stranding network operating along this coast, the most common stranding events comprise six cetacean species (Delphinus delphis, Tursiops truncatus, Stenella coeruleoalba, Globicephala melas, Grampus griseus, Phocoena phocoena)and one pinniped species (Halichoerus grypus). Rare stranding events include deep-diving or exotic species, such as arctic seals. In this study, our aim was to determine the potential contribution of DNA barcoding to the monitoring of marine mammal biodiversity as performed by the stranding network.
We sequenced more than 500 bp of the 5’ end of the mitochondrial COI gene of 89 animals of 15 different species (12 cetaceans, and three pinnipeds). Except for members of the Delphininae, all species were unambiguously discriminated on the basis of their COI sequences. We then applied DNA barcoding to identify some “undetermined” samples. With again the exception of the Delphininae, this was successful using the BOLD identification engine. For samples of the Delphininae, we sequenced a portion of the mitochondrial control region (MCR), and using a non-metric multidimentional scaling plot and posterior probability calculations we were able to determine putatively each species. We then showed, in the case of the harbour porpoise, that COI polymorphisms, although being lower than MCR ones, could also be used to assess intraspecific variability. All these results show that the use of DNA barcoding in conjunction with a stranding network could clearly increase the accuracy of the monitoring of marine mammal biodiversity.
doi:10.3897/zookeys.365.5873
PMCID: PMC3890668  PMID: 24453548
DNA barcoding; COI; control region; marine mammals; cetaceans; pinnipeds; biodiversity monitoring; stranding network
21.  Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews 
Aquatic Biosystems  2012;8:3.
Background
Killer whales (Orcinus orca) are the most widely distributed cetacean, occurring in all oceans worldwide, and within ocean regions different ecotypes are defined based on prey preferences. Prey items are largely unknown in the eastern Canadian Arctic and therefore we conducted a survey of Inuit Traditional Ecological Knowledge (TEK) to provide information on the feeding ecology of killer whales. We compiled Inuit observations on killer whales and their prey items via 105 semi-directed interviews conducted in 11 eastern Nunavut communities (Kivalliq and Qikiqtaaluk regions) from 2007-2010.
Results
Results detail local knowledge of killer whale prey items, hunting behaviour, prey responses, distribution of predation events, and prey capture techniques. Inuit TEK and published literature agree that killer whales at times eat only certain parts of prey, particularly of large whales, that attacks on large whales entail relatively small groups of killer whales, and that they hunt cooperatively. Inuit observations suggest that there is little prey specialization beyond marine mammals and there are no definitive observations of fish in the diet. Inuit hunters and elders also documented the use of sea ice and shallow water as prey refugia.
Conclusions
By combining TEK and scientific approaches we provide a more holistic view of killer whale predation in the eastern Canadian Arctic relevant to management and policy. Continuing the long-term relationship between scientists and hunters will provide for successful knowledge integration and has resulted in considerable improvement in understanding of killer whale ecology relevant to management of prey species. Combining scientists and Inuit knowledge will assist in northerners adapting to the restructuring of the Arctic marine ecosystem associated with warming and loss of sea ice.
doi:10.1186/2046-9063-8-3
PMCID: PMC3310332  PMID: 22520955
beluga whales; bowhead whales; group size; hunting behaviour; narwhal whales; predator-prey relations; prey capture techniques; Traditional Ecological Knowledge; seals; walrus
22.  Submarine canyons: hotspots of benthic biomass and productivity in the deep sea 
Submarine canyons are dramatic and widespread topographic features crossing continental and island margins in all oceans. Canyons can be sites of enhanced organic-matter flux and deposition through entrainment of coastal detrital export, dense shelf-water cascade, channelling of resuspended particulate material and focusing of sediment deposition. Despite their unusual ecological characteristics and global distribution along oceanic continental margins, only scattered information is available about the influence of submarine canyons on deep-sea ecosystem structure and productivity. Here, we show that deep-sea canyons such as the Kaikoura Canyon on the eastern New Zealand margin (42°01′ S, 173°03′ E) can sustain enormous biomasses of infaunal megabenthic invertebrates over large areas. Our reported biomass values are 100-fold higher than those previously reported for deep-sea (non-chemosynthetic) habitats below 500 m in the ocean. We also present evidence from deep-sea-towed camera images that areas in the canyon that have the extraordinary benthic biomass also harbour high abundances of macrourid (rattail) fishes likely to be feeding on the macro- and megabenthos. Bottom-trawl catch data also indicate that the Kaikoura Canyon has dramatically higher abundances of benthic-feeding fishes than adjacent slopes. Our results demonstrate that the Kaikoura Canyon is one of the most productive habitats described so far in the deep sea. A new global inventory suggests there are at least 660 submarine canyons worldwide, approximately 100 of which could be biomass hotspots similar to the Kaikoura Canyon. The importance of such deep-sea canyons as potential hotspots of production and commercial fisheries yields merits substantial further study.
doi:10.1098/rspb.2010.0462
PMCID: PMC2981985  PMID: 20444722
submarine canyons; benthic biomass hotspots; molpadiid holothurians; macrourid fishes; eastern New Zealand margin
23.  Seasonal Movements, Aggregations and Diving Behavior of Atlantic Bluefin Tuna (Thunnus thynnus) Revealed with Archival Tags 
PLoS ONE  2009;4(7):e6151.
Electronic tags were used to examine the seasonal movements, aggregations and diving behaviors of Atlantic bluefin tuna (Thunnus thynnus) to better understand their migration ecology and oceanic habitat utilization. Implantable archival tags (n = 561) were deployed in bluefin tuna from 1996 to 2005 and 106 tags were recovered. Movement paths of the fish were reconstructed using light level and sea-surface-temperature-based geolocation estimates. To quantify habitat utilization we employed a weighted kernel estimation technique that removed the biases of deployment location and track length. Throughout the North Atlantic, high residence times (167±33 days) were identified in four spatially confined regions on a seasonal scale. Within each region, bluefin tuna experienced distinct temperature regimes and displayed different diving behaviors. The mean diving depths within the high-use areas were significantly shallower and the dive frequency and the variance in internal temperature significantly higher than during transit movements between the high-use areas. Residence time in the more northern latitude high-use areas was significantly correlated with levels of primary productivity. The regions of aggregation are associated with areas of abundant prey and potentially represent critical foraging habitats that have seasonally abundant prey. Throughout the North Atlantic mean diving depth was significantly correlated with the depth of the thermocline, and dive behavior changed in relation to the stratification of the water column. In this study, with numerous multi-year tracks, there appear to be repeatable patterns of clear aggregation areas that potentially are changing with environmental conditions. The high concentrations of bluefin tuna in predictable locations indicate that Atlantic bluefin tuna are vulnerable to concentrated fishing efforts in the regions of foraging aggregations.
doi:10.1371/journal.pone.0006151
PMCID: PMC2701635  PMID: 19582150
24.  Wide Range of Mercury Contamination in Chicks of Southern Ocean Seabirds 
PLoS ONE  2013;8(1):e54508.
Using top predators as sentinels of the marine environment, Hg contamination was investigated within the large subantarctic seabird community of Kerguelen Islands, a remote area from the poorly known Southern Indian Ocean. Chicks of 21 sympatric seabirds presented a wide range of Hg concentrations, with the highest contaminated species containing ∼102 times more feather Hg than the less contaminated species. Hence, Kerguelen seabirds encompass the whole range of chick feather Hg values that were previously collected worldwide in poorly industrialized localities. Using stable isotopes, the effects of foraging habitats (reflected by δ13C) and trophic positions (reflected by δ15N) on Hg concentrations were investigated. Species-related Hg variations were highly and positively linked to feather δ15N values, thus highlighting the occurrence of efficient Hg biomagnification processes within subantarctic marine trophic webs. By contrast, Hg contamination overall correlated poorly with feeding habitats, because of the pooling of species foraging within different isotopic gradients corresponding to distinct seabird habitats (benthic, pelagic, neritic and oceanic). However, when focusing on oceanic seabirds, Hg concentration was related to feather δ13C values, with species feeding in colder waters (lower δ13C values) south of Kerguelen Islands being less prone to be contaminated than species feeding in northern warmer waters (higher δ13C values). Within the context of continuous increase in global Hg emissions, Kerguelen Islands that are located far away from anthropogenic sources can be considered as an ideal study site to monitor the temporal trend of global Hg contamination. The present work helps selecting some seabird species as sentinels of environmental pollution according to their high Hg concentrations and their contrasted foraging ecology.
doi:10.1371/journal.pone.0054508
PMCID: PMC3547921  PMID: 23349912
25.  What Happened to Gray Whales during the Pleistocene? The Ecological Impact of Sea-Level Change on Benthic Feeding Areas in the North Pacific Ocean 
PLoS ONE  2011;6(7):e21295.
Background
Gray whales (Eschrichtius robustus) undertake long migrations, from Baja California to Alaska, to feed on seasonally productive benthos of the Bering and Chukchi seas. The invertebrates that form their primary prey are restricted to shallow water environments, but global sea-level changes during the Pleistocene eliminated or reduced this critical habitat multiple times. Because the fossil record of gray whales is coincident with the onset of Northern Hemisphere glaciation, gray whales survived these massive changes to their feeding habitat, but it is unclear how.
Methodology/Principal Findings
We reconstructed gray whale carrying capacity fluctuations during the past 120,000 years by quantifying gray whale feeding habitat availability using bathymetric data for the North Pacific Ocean, constrained by their maximum diving depth. We calculated carrying capacity based on modern estimates of metabolic demand, prey availability, and feeding duration; we also constrained our estimates to reflect current population size and account for glaciated and non-glaciated areas in the North Pacific. Our results show that key feeding areas eliminated by sea-level lowstands were not replaced by commensurate areas. Our reconstructions show that such reductions affected carrying capacity, and harmonic means of these fluctuations do not differ dramatically from genetic estimates of carrying capacity.
Conclusions/Significance
Assuming current carrying capacity estimates, Pleistocene glacial maxima may have created multiple, weak genetic bottlenecks, although the current temporal resolution of genetic datasets does not test for such signals. Our results do not, however, falsify molecular estimates of pre-whaling population size because those abundances would have been sufficient to survive the loss of major benthic feeding areas (i.e., the majority of the Bering Shelf) during glacial maxima. We propose that gray whales survived the disappearance of their primary feeding ground by employing generalist filter-feeding modes, similar to the resident gray whales found between northern Washington State and Vancouver Island.
doi:10.1371/journal.pone.0021295
PMCID: PMC3130736  PMID: 21754984

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