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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.
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.
PMCID: PMC3367652  PMID: 16485476
Bartonella; cetacean; porpoise; emerging; stranded; research
3.  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.
PMCID: PMC2981983  PMID: 20444724
cetacean; climate change; habitat fragmentation; population genetics; coalescence
4.  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.
PMCID: PMC3287339  PMID: 22393524
Climate change; harbour porpoise; west greenland; body condition; Atlantic cod
5.  Zn, Cu, Cd and Hg binding to metallothioneins in harbour porpoises Phocoena phocoena from the southern North Sea 
BMC Ecology  2006;6:2.
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.
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.
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.
PMCID: PMC1434725  PMID: 16464247
6.  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.
PMCID: PMC3632559  PMID: 23614031
7.  Bivalves as indicators of environmental variation and potential anthropogenic impacts in the southern Barents Sea 
Marine pollution bulletin  2009;59(4-7):193-206.
Identifying patterns and drivers of natural variability in populations is necessary to gauge potential effects of climatic change and the expected increases in commercial activities in the Arctic on communities and ecosystems. We analyzed growth rates and shell geochemistry of the circumpolar Greenland smooth cockle, Serripes groenlandicus, from the southern Barents Sea over almost 70 years between 1882 and 1968. The datasets were calibrated via annually-deposited growth lines, and growth, stable isotope (δ18O, δ13C), and trace elemental (Mg, Sr, Ba, Mn) patterns were linked to environmental variations on weekly to decadal scales. Standardized growth indices revealed an oscillatory growth pattern with a multi-year periodicity, which was inversely related to the North Atlantic Oscillation Index (NAO), and positively related to local river discharge. Up to 60% of the annual variability in the Ba/Ca could be explained by variations in river discharge at the site closest to the rivers, but the relationship disappeared at a more distant location. Patterns of δ18O, δ13C, and Sr/Ca together provide evidence that bivalve growth ceases at elevated temperatures during the fall and recommences at the coldest temperatures in the early spring, with the implication that food, rather than temperature, is the primary driver of bivalve growth. The multi-proxy approach of combining the annually integrated information from the growth results and higher resolution geochemical results yielded a robust interpretation of biophysical coupling in the region over temporal and spatial scales. We thus demonstrate that sclerochronological proxies can be useful retrospective analytical tools for establishing a baseline of ecosystem variability in assessing potential combined impacts of climatic change and increasing commercial activities on Arctic communities.
PMCID: PMC2707507  PMID: 19394657
Arctic; Barents Sea; benthic community; bivalve growth; climate oscillation; environmental forcing; North Atlantic Oscillation; White Sea; sclerochronology; Serripes groenlandicus; shell geochemistry; stable isotopes; trace element ratios
8.  Evaluation of immune and stress status in harbour porpoises (Phocoena phocoena): can hormones and mRNA expression levels serve as indicators to assess stress? 
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.
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.
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.
PMCID: PMC3734172  PMID: 23866055
Harbour porpoise; Stress hormones; Cytokines; Anthropogenic impact; Offshore wind farms; Underwater noise
9.  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.
PMCID: PMC2375924  PMID: 17251125
harbour porpoise; sandeels; climate change
10.  Locations of marine animals revealed by carbon isotopes 
Scientific Reports  2011;1:21.
Knowing the distribution of marine animals is central to understanding climatic and other environmental influences on population ecology. This information has proven difficult to gain through capture-based methods biased by capture location. Here we show that marine location can be inferred from animal tissues. As the carbon isotope composition of animal tissues varies with sea surface temperature, marine location can be identified by matching time series of carbon isotopes measured in tissues to sea surface temperature records. Applying this technique to populations of Atlantic salmon (Salmo salar L.) produces isotopically-derived maps of oceanic feeding grounds, consistent with the current understanding of salmon migrations, that additionally reveal geographic segregation in feeding grounds between individual philopatric populations and age-classes. Carbon isotope ratios can be used to identify the location of open ocean feeding grounds for any pelagic animals for which tissue archives and matching records of sea surface temperature are available.
PMCID: PMC3216509  PMID: 22355540
11.  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.
PMCID: PMC3899228  PMID: 24466031
12.  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.
PMCID: PMC3440431  PMID: 22984507
13.  Ten Years after the Prestige Oil Spill: Seabird Trophic Ecology as Indicator of Long-Term Effects on the Coastal Marine Ecosystem 
PLoS ONE  2013;8(10):e77360.
Major oil spills can have long-term impacts since oil pollution does not only result in acute mortality of marine organisms, but also affects productivity levels, predator-prey dynamics, and damages habitats that support marine communities. However, despite the conservation implications of oil accidents, the monitoring and assessment of its lasting impacts still remains a difficult and daunting task. Here, we used European shags to evaluate the overall, lasting effects of the Prestige oil spill (2002) on the affected marine ecosystem. Using δ15N and Hg analysis, we trace temporal changes in feeding ecology potentially related to alterations of the food web due to the spill. Using climatic and oceanic data, we also investigate the influence of North Atlantic Oscillation (NAO) index, the sea surface temperature (SST) and the chlorophyll a (Chl a) on the observed changes. Analysis of δ15N and Hg concentrations revealed that after the Prestige oil spill, shag chicks abruptly switched their trophic level from a diet based on a high percentage of demersal-benthic fish to a higher proportion of pelagic/semi-pelagic species. There was no evidence that Chl a, SST and NAO reflected any particular changes or severity in environmental conditions for any year or season that may explain the sudden change observed in trophic level. Thus, this study highlighted an impact on the marine food web for at least three years. Our results provide the best evidence to date of the long-term consequences of the Prestige oil spill. They also show how, regardless of wider oceanographic variability, lasting impacts on predator-prey dynamics can be assessed using biochemical markers. This is particularly useful if larger scale and longer term monitoring of all trophic levels is unfeasible due to limited funding or high ecosystem complexity.
PMCID: PMC3793948  PMID: 24130877
14.  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.
PMCID: PMC3923852  PMID: 24551217
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.
PMCID: PMC3960146  PMID: 24646920
16.  Individual specialists in a generalist population: results from a long-term stable isotope series 
Biology Letters  2010;6(5):711-714.
Individual variation in resource use has often been ignored in ecological studies, but closer examination of individual patterns through time may reveal significant intrapopulation differences. Adult loggerhead sea turtles (Caretta caretta) are generalist carnivores with a wide geographical range, resulting in a broad isotopic niche. We microsampled scute, a persistent and continuously growing tissue, to examine long-term variation in resource use (up to 12 years) in 15 nesting loggerhead turtles. Using stable isotopes of nitrogen and carbon, we examined the resource use patterns (integration of diet, habitat and geographical location) and demonstrate that individual loggerheads are long-term specialists within a generalist population. We present our results in the context of a conceptual model comparing isotopic niches in specialist and generalist populations. Individual consistency may have important ecological, evolutionary and conservation consequences, such as the reduction of intraspecific competition.
PMCID: PMC2936143  PMID: 20335202
isotopic niche; resource use; sea turtles; specialist; stable isotopes
17.  Ecosystem Services Transcend Boundaries: Estuaries Provide Resource Subsidies and Influence Functional Diversity in Coastal Benthic Communities 
PLoS ONE  2012;7(8):e42708.
Estuaries are highly productive ecosystems that can export organic matter to coastal seas (the ‘outwelling hypothesis’). However the role of this food resource subsidy on coastal ecosystem functioning has not been examined.
Methodology/Principal Findings
We investigated the influence of estuarine primary production as a resource subsidy and the influence of estuaries on biodiversity and ecosystem functioning in coastal mollusk-dominated sediment communities. Stable isotope values (δ13C, δ15N) demonstrated that estuarine primary production was exported to the adjacent coast and contributed to secondary production up to 4 km from the estuary mouth. Further, isotope signatures of suspension feeding bivalves on the adjacent coast (Dosinia subrosea) closely mirrored the isotope values of the dominant bivalves inside the estuaries (Austrovenus stutchburyi), indicating utilization of similar organic matter sources. However, the food subsidies varied between estuaries; with estuarine suspended particulate organic matter (SPOM) dominant at Tairua estuary, while seagrass and fringing vegetation detritus was proportionately more important at Whangapoua estuary, with lesser contributions of estuarine SPOM. Distance from the estuary mouth and the size and density of large bivalves (Dosinia spp.) had a significant influence on the composition of biological traits in the coastal macrobenthic communities, signaling the potential influence of these spatial subsidies on ecosystem functioning.
Our study demonstrated that the locations where ecosystem services like productivity are generated are not necessarily where the services are utilized. Further, we identified indirect positive effects of the nutrient subsidies on biodiversity (the estuarine subsidies influenced the bivalves, which in turn affected the diversity and functional trait composition of the coastal sediment macrofaunal communities). These findings highlight the importance of integrative ecosystem-based management that maintains the connectivity of estuarine and coastal ecosystems.
PMCID: PMC3411827  PMID: 22880089
18.  Brucella ceti Infection in Harbor Porpoise (Phocoena phocoena) 
Emerging Infectious Diseases  2010;16(12):1966-1968.
We describe Brucella sp. infection and associated lesions in a harbor porpoise (Phocoena phocoena) found on the coast of Belgium. The infection was diagnosed by immunohistochemistry, transmission electron microscopy, and bacteriology, and the organism was identified as B. ceti. The infection’s location in the porpoise raises questions of abortion and zoonotic risks.
PMCID: PMC3294555  PMID: 21122233
Bacteria; zoonoses; Brucella ceti; cetaceans; harbor porpoise; brucellosis; dispatch
19.  Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds 
Biology Letters  2006;2(2):301-303.
Although there is increasing evidence that climatic variations during the non-breeding season shape population dynamics of seabirds, most aspects of their winter distribution and ecology remain essentially unknown. We used stable isotope signatures in feathers to infer and compare the moulting (wintering) habitat of subantarctic petrels breeding at two distant localities (South Georgia and Kerguelen). Petrels showed species-specific wintering habitat preferences, with a similar pattern of latitudinal segregation for all but one taxon. At both localities, δ13C values indicated that blue petrels (Halobaena caerulea) moult in Antarctic waters, South Georgian diving petrels (Pelecanoides georgicus) in the vicinity of the archipelagos and/or in the Polar Frontal Zone and Antarctic prions (Pachyptila desolata) in warmer waters. In contrast, common diving petrels (Pelecanoides urinatrix) showed divergent strategies, with low and high intrapopulation variation at South Georgia and Kerguelen, respectively. Birds from Kerguelen dispersed over a much wider range of habitats, from coastal to oceanic waters and from Antarctica to the subtropics, whereas those from South Georgia wintered mainly in waters around the archipelago. This study is the first to show such striking between-population heterogeneity in individual wintering strategies, which could have important implications for likely demographic responses to environmental perturbation.
PMCID: PMC1618904  PMID: 17148388
moulting period; individual specialization; procellariiform seabird; Southern Ocean; Antarctica
20.  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.
PMCID: PMC2275888  PMID: 17698485
energy reserves; starvation risk; starvation–predation risk trade-off; Phocoena phocoena; Tursiops truncatus
21.  Keeping returns optimal: gain control exerted through sensitivity adjustments in the harbour porpoise auditory system 
Animals that use echolocation (biosonar) listen to acoustic signals with a large range of intensities, because echo levels vary with the fourth power of the animal's distance to the target. In man-made sonar, engineers apply automatic gain control to stabilize the echo energy levels, thereby rendering them independent of distance to the target. Both toothed whales and bats vary the level of their echolocation clicks to compensate for the distance-related energy loss. By monitoring the auditory brainstem response (ABR) during a psychophysical task, we found that a harbour porpoise (Phocoena phocoena), in addition to adjusting the sound level of the outgoing signals up to 5.4 dB, also reduces its ABR threshold by 6 dB when the target distance doubles. This self-induced threshold shift increases the dynamic range of the biosonar system and compensates for half of the variation of energy that is caused by changes in the distance to the target. In combination with an increased source level as a function of target range, this helps the porpoise to maintain a stable echo-evoked ABR amplitude irrespective of target range, and is therefore probably an important tool enabling porpoises to efficiently analyse and classify received echoes.
PMCID: PMC3321710  PMID: 22279169
auditory brainstem response; ABR threshold; automatic gain control; dynamic range
22.  Trace Elements and Carbon and Nitrogen Stable Isotopes in Organisms from a Tropical Coastal Lagoon 
Trace elements (Fe, Mn, Al, Zn, Cr, Cu, Ni, Pb, Cd, Hg, and As) and stable isotope ratios (δ13C and δ15N) were analyzed in sediments, invertebrates, and fishes from a tropical coastal lagoon influenced by iron ore mining and processing activities to assess the differences in trace element accumulation patterns among species and to investigate relations with trophic levels of the organisms involved. Overall significant negative relations between trophic level (given by 15N) and trace element concentrations in gastropods and crustaceans showed differences in internal controls of trace element accumulation among the species of different trophic positions, leading to trace element dilution. Generally, no significant relation between δ15N and trace element concentrations was observed among fish species, probably due to omnivory in a number of species as well as fast growth. Trace element accumulation was observed in the fish tissues, with higher levels of most trace elements found in liver compared with muscle and gill. Levels of Fe, Mn, Al, and Hg in invertebrates, and Fe and Cu in fish livers, were comparable with levels in organisms and tissues from other contaminated areas. Trace element levels in fish muscle were below the international safety baseline standards for human consumption.
PMCID: PMC2928917  PMID: 20217062
23.  Tracing early stages of species differentiation: Ecological, morphological and genetic divergence of Galápagos sea lion populations 
Oceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation.
We find significant ecological, morphological and genetic divergence between the western colonies and colonies from the central region of the archipelago that are exposed to different ecological conditions. Stable isotope analyses indicate that western animals use different food sources than those from the central area. This is likely due to niche partitioning with the second Galápagos eared seal species, the Galápagos fur seal (Arctocephalus galapagoensis) that exclusively dwells in the west. Stable isotope patterns correlate with significant differences in foraging-related skull morphology. Analyses of mitochondrial sequences as well as microsatellites reveal signs of initial genetic differentiation.
Our results suggest a key role of intra- as well as inter-specific niche segregation in the evolution of genetic structure among populations of a highly mobile species under conditions of free movement. Given the monophyletic arrival of the sea lions on the archipelago, our study challenges the view that geographical barriers are strictly needed for the build-up of genetic divergence. The study further raises the interesting prospect that in social, colonially breeding mammals additional forces, such as social structure or feeding traditions, might bear on the genetic partitioning of populations.
PMCID: PMC2408593  PMID: 18485220
24.  A Stable-Isotope Mass Spectrometry-Based Metabolic Footprinting Approach to Analyze Exudates from Phytoplankton 
Marine Drugs  2013;11(11):4158-4175.
Phytoplankton exudates play an important role in pelagic ecology and biogeochemical cycles of elements. Exuded compounds fuel the microbial food web and often encompass bioactive secondary metabolites like sex pheromones, allelochemicals, antibiotics, or feeding attractants that mediate biological interactions. Despite this importance, little is known about the bioactive compounds present in phytoplankton exudates. We report a stable-isotope metabolic footprinting method to characterise exudates from aquatic autotrophs. Exudates from 13C-enriched alga were concentrated by solid phase extraction and analysed by high-resolution Fourier transform ion cyclotron resonance mass spectrometry. We used the harmful algal bloom forming dinoflagellate Alexandrium tamarense to prove the method. An algorithm was developed to automatically pinpoint just those metabolites with highly 13C-enriched isotope signatures, allowing us to discover algal exudates from the complex seawater background. The stable-isotope pattern (SIP) of the detected metabolites then allowed for more accurate assignment to an empirical formula, a critical first step in their identification. This automated workflow provides an effective way to explore the chemical nature of the solutes exuded from phytoplankton cells and will facilitate the discovery of novel dissolved bioactive compounds.
PMCID: PMC3853721  PMID: 24172212
metabolomics; stable isotope; algal exudate; dinoflagellate; correlation analysis; DIMS; exometabolome; FT-ICR; 13C; chemical ecology
25.  Stable platinum isotope measurements in presolar nanodiamonds by TEAMS 
Nanodiamonds are stardust grains commonly found in primitive meteorites. They survived the formation of the solar system and kept their own individuality. Measurements of trace-element isotopic signatures in these grains will help understanding heavy element nucleosynthesis in massive stars and dust formation from their ejecta. We have continued previous attempts to search for stable Pt isotope anomalies in nanodiamonds via trace element accelerator mass spectrometry (TEAMS). The installation of a new injector beam line at the VERA facility allowed studying low traces of stable elements in different materials. Moreover, recent experiments showed that VERA provides the required measurement precision together with a low Pt machine background. Here, we observed for the first time an indication for enhancements of 198Pt/195Pt isotope ratios in two diamond residues prepared by different chemical separation techniques from the Allende meteorite. Variations in other isotopic ratios were within analytical uncertainty, and no anomaly was identified in a third diamond fraction.
PMCID: PMC3617595  PMID: 23565017
TEAMS; Trace elements; Pt; Super novae; Presolar grains; Nanodiamonds

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