stranded porpoise, Ireland BIOCET

Bioaccumulation of Persistent Organic Pollutants in Small Cetaceans in European Waters: Transport Pathways and Impact on Reproduction


This site contains information about the project BIOCET, funded during 2001-04 under the EC's ENERGY, ENVIRONMENT AND SUSTAINABLE DEVELOPMENT programme (contract number EVK3 - 2000 - 00027). BIOCET was part of the IMPACTS cluster of projects. The work carried out was based on samples collected from dead cetaceans washed up on the seashore (strandings), which were used to identify links between diet, bioaccumulation of contaminants, and reproductive success.

Last updated: 26/07/06


Contents

 

Project summary

Publications

Work programme

Partners

Collaborations

The Impacts cluster

Gallery 1 - Leiden 2002

Gallery 2 La Rochelle 2004

Web page for project partners (password access)

 

 stranded common dolphin, Galicia

Project Executive Summary

Objectives

This project aimed to quantify and model the process and time-course of bioaccumulation of persistent organic pollutants (POPs) in small cetaceans (focusing primarily on female common dolphins Delphinus delphis and harbour porpoises Phocoena phocoena) in NE Atlantic waters. This involved collecting individual-level and population-level datasets for use in comparisons and models. Seven partner institutions in five European countries worked over three years on nine workpackages. Data were collected on histopathology, reproduction, age, diet, inorganic pollutants and POPs. The objectives of the project were then to:

· Identify and model pathways of POP bioaccumulation· Identify trophic links contributing to bioaccumulation

· Compare reproductive success between populations· Identify areas in which the cetaceans studied are vulnerable to effects of bioaccumulation

· Compare reproductive success between individual females, in relation to age and diet

· Quantify and model the time-course of bioaccumulation in female porpoises and dolphins

· Provide synthesis and recommendations on issues related to the conservation of small cetaceans and the management of pollution in coastal zone and oceanic waters

· Disseminate and publish results on these studies

Scientific achievements

Co-ordination (WP1): Calibration workshops were held to ensure harmonised data collection and analysis. The project website has been updated (http://www.abdn.ac.uk/biocet) and project work has already appeared in several publications and conference presentations. Sample material has been preserved in sample banks. All project data have been put together in a series of linked databases that will ultimately become more widely available.

Sampling (WP2): Sample collection extended over almost 2.5 years, accessing stranded and by-caught cetaceans through local strandings schemes, as well as sampling prey species.

Pathology (WP3): There was considerable geographic variation in causes of mortality, e.g. the relative importance of pathological causes and fishery by-catch. There was evidence of Brucella infection in the Dutch and Scottish harbour porpoise populations. Only for Belgium has little evidence of Brucella been found despite testing for it.

Age (WP4): Age readings were completed and used to derive growth curves for three species. A CD-ROM of images to assist future practical work was prepared. There were regional differences in sample age structure for common dolphins and harbour porpoises, with a preponderance of old animals in the Dutch porpoise population.

Reproduction (WP5): Reproductive status was determined for all studied animals, and counts and measurements on ovarian scars were taken for target individuals. Age at sexual maturity and pregnancy rates were derived for each population. Several lines of evidence indicate that corpora scars do not usually provide a reliable indicator of past pregnancies in small cetaceans. The pregnancy rate in Dutch harbour porpoises was especially low.

Diet (WP6). Stomach contents were analysed when available and analysis of blubber fatty acid profiles was completed for all target animals and selected prey species. Fatty acid profiles showed seasonal, regional, ontogenetic and interspecific variation, some trends being readily interpretable in terms of likely dietary variation. Quantitative fatty acid analysis allowed average diets to be predicted. However, cetacean fatty acid profiles are distinct from those of most putative prey and further calibration is needed.

Persistent organic pollutants (WP7): POP analyses were completed (in collaboration with CEFAS and the UK Strandings Project for UK samples) on all target animals and selected prey species, including determinations of the relatively new brominated flame retardant (BFR) hexabromocyclo-dodecane (HBCD) (not mentioned in the contract). HBCD is a high production volume (9500 tons within the EU in 2001) BFR used in the building industry. Highest HBCD levels occurred in harbour porpoises stranded on the coasts of the Irish Sea and the NW coast of Scotland, but the residues contained exclusively the relatively uncommon a-isomer. Levels of tributyltin in liver of harbour porpoises from the North Sea ranged at the highest end of levels reported. Median levels of S18-PCBs and CB153 in harbour porpoises from the southern North Sea, and common dolphins from the Western Channel and the Bay of Biscay were above the threshold levels for effects on reproduction as reported in the literature for the bottlenose dolphin and the harbour seal.

Toxic elements (WP8): As for WP7, some analyses were carried out in collaboration with CEFAS (UK) and both cetacean tissues (kidney, liver) and prey were analysed. Levels of mercury in liver and cadmium in kidney correlated well with age in a group of common dolphins that mass-stranded on the coast of Brittany (France). A strong relationship between age and mercury was seen in most studied small cetacean populations, although regional differences were also seen.

Synthesis (WP9). POP levels in female common dolphins were shown to be linked to diet, area and reproductive status, although not related to age; results for harbour porpoises indicated only area effects. Cadmium concentrations appeared to be closely linked to diet. The number of scars recorded on common dolphin ovaries was correlated with mercury burdens, and to a lesser extent to POP burdens and diet. Transfers of organic and metallic pollutants via food were estimated.

Socio-economic relevance and policy implications

The project is relevant to the conservation of small cetaceans and the management of pollution in coastal zone and oceanic waters. Porpoises and dolphins eat fish and invertebrates (e.g. squid and octopus) that are also eaten by man. Effects on reproduction in cetaceans provide a possible model for effects that might be seen in human communities with a substantial per-capita consumption of seafood. The study has highlighted areas where cetaceans carry high burdens of pollutants, levels sometimes exceeding those known to affect reproduction. Pregnancy rate in Dutch harbour porpoises was particularly low and, taken together with high PCB levels, skewed age structure and presence of Brucella, suggests that this population is particularly at risk. The PBDEs found were exclusively tetra- to hexa-BDEs that are prominent in the commercial penta-formulation. This proves that the EU has been right in focussing its main restrictive policy on this mixture.

Keywords: Cetaceans, persistent organic pollutants, bioaccumulation, reproduction

Publications

Publications from the BIOCET programme will be listed here, where possible in downloadable form.

Caurant, F., Aubail, A., Lahaye, V., Van Canneyt, O., Rogan, E., López, A., Addink, M., Churlaud, C., Robert, M. & Bustamante, P., 2006. Lead contamination of small cetaceans in European waters - the use of stable isotopes for identifying the sources of lead exposure. Marine Environmental Research 62, 131-148.

Lahaye, V., Bustamante, P., Dabin, W., Van Canneyt, O., Dhermain, F., Cesarini, C., Pierce, G.J. & Caurant, F., 2006. New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean waters. Marine Pollution Bulletin

Lahaye, V., Bustamante, P., Spitz, J., Dabin, W., Das, K., Pierce, G.J. & Caurant, F., 2005. Long-term dietary segregation of common dolphins (Delphinus delphis) in the Bay of Biscay, determined using cadmium as an ecological tracer. Marine Ecology Progress Series 305, 275-285.

Murphy, S., Herman, J., Pierce, G.J., Rogan, E. & Kitchener, A., 2006. Taxonomic status and geographical cranial variation of common dolphins (Delphinus) in the eastern north Atlantic. Marine Mammal Science 22, 573-599.

Pierce, G.J., Santos, M.B., Reid, R.J., Patterson, I.A.P. & Ross, H.M., 2004. Diet of minke whales Balaenoptera acutorostrata in Scottish (UK) waters with notes on strandings of this species in Scotland 1992-2002. Journal of the Marine Biological Association of the United Kingdom 84, 1241-1244.

Santos, M.B. & Pierce, G.J., 2003. The diet of harbour porpoise (Phocoena phocoena) in the Northeast Atlantic. Oceanography & Marine Biology: An Annual Review 41, 355-390.

Santos, M.B., Pierce, G.J., Learmonth, J.A., Reid, R.J., Ross, H.M., Patterson, I.A.P., Reid D.G. & Beare, D., 2004. Variability in the diet of harbour porpoises (Phocoena phocoena) in Scottish waters 1992-2003. Marine Mammal Science 20, 1-27.

Spitz, J., Richard, E., Meynier, L., Pusineri, C. & Ridoux, V., 2006. Dietary plasticity of the oceanic striped dolphin, Stenella coeruleoalba, in the neritic waters of the Bay of Biscay. Journal of Sea Research 55, 309-320.

Zegers, B.N., Mets, A., Van Bommel, R., Minkenberg, C., Hamers, T., Kamstra, J.H., Pierce, G.J. & Boon, J.P., 2005. Levels of hexabromocyclododecane in harbor porpoises and common dolphins from Western European seas, with evidence for stereoisomer-specific biotransformation by cytochrome P450. Environmental Science and Technology 39, 2095-2100.

 

Work programme

1. CO-ORDINATION AND DISSEMINATION – leader UNIABDN (Graham Pierce)

Monitoring and management of scientific progress and general day-to-day communication within the project. Workshops for different aspects of the research, annual co-ordination meetings, co-ordination of the production of deliverables and other project publications. Ensures harmonisation of data collection.

2. SAMPLING AND NECROPSY – leader NNM (Chris Smeenk)

Sampling and basic data collection, on cetaceans and their prey, underpinning work-packages 3 - 9. Data collection is carried out in association with local/national strandings networks. A workshop on sampling and necropsy procedures took place in month 2 to review and harmonise data collection.

3. VETERINARY HISTOPATHOLOGY, BACTERIOLOGY AND VIROLOGY – leader NNM (Manuel Garica Hartmann)

The impact of POPs on reproduction may be indirect, e.g. by depressing the immune system they may increase susceptibility to disease (Jepson et al., 1999). Diseases may on the other hand affect the impact of POPs. Samples of major organs will be taken for histopathological analysis. Examination of lesions where bacterial and or viral causes are suspected and sampling for later analysis, following standard methodology developed by the European Cetacean Society (Kuiken & García Hartmann, 1993). Especial care will be taken to try to identify evidence of reproductive pathology.

4. MEASUREMENT OF AGE – leader UCC (Emer Rogan)

Estimation of age is essential for interpreting the data collected in other workpackages, especially on reproductive output and contaminant burdens. It will be a fundamental parameter of the models to be produced. This will allow determination of the time course of bioaccumulation, and of any detrimental effects on reproduction, both for individuals and for an average animal in each population. Age will be determined for all cetaceans sampled. Workshops for harmonisation of techniques and validation of results were held in project months 9 and 14.

5. MEASUREMENT OF REPRODUCTIVE OUTPUT – leader NNM (Marjan Addink)

The best available measure of fitness is lifetime reproductive output. Estimation of an index of lifetime reproductive output will be attempted at both population and individual levels. There is evidence that the age at sexual maturity (ASM) of female porpoises varies between populations. If the ASM is relatively high, females accumulate more pollutants before their first pregnancy, which can mean higher levels passed on to their first calf. By examining the number of pregnant and lactating females in a sample group we can calculate a pregnancy rate. An index of the number of past pregnancies (IPP) for an individual may be derived by counting the number of corpora albicantia (CA) in the ovaries (Perrin et al., 1984). Some porpoises undergo multiple ovulations when first starting to ovulate but the place in the ovary where this happens can often be distinguished. There is evidence that bioaccumulation of contaminants may block ovulation (De Guise & Béland, 1994).

It is anticipated that reproductive material from all females collected will be examined. Workshops for harmonisation of techniques and validation of results were held in project months 9 and 14.

6. DIET ANALYSIS – leader UNIABDN (Begoña Santos)

The major route of entry of contaminants, after the initial maternal transfer, is expected to be in food. The choice of diet of each species, and of each population and individual may therefore determine the rate at which contaminants are bio-accumulated. Based on quantitative data on the diet (this study and literature) and energy requirements (literature values), it should be possible to predict the rate of INPUT of contaminants for each species, population group and, ultimately, individual. Information on diet will be gathered from literature, new stomach contents analysis and fatty acid analysis of blubber samples. Stomach contents provide less useful information on diet at the individual level and, for this reason, fatty acid analysis is also used. Most mammalian fatty acids are derived from their food and the inner blubber of cetaceans is thought to be mainly of dietary origin.

It is anticipated that dietary material from all cetaceans collected will be examined. A workshop for harmonisation of techniques and validation of results was held after 14 months.

7. MEASUREMENT OF POP LEVELS IN CETACEAN AND PREY TISSUES – leader NIOZ (Jan Boon)

There is abundant evidence that (a) pollution of the marine environment with organic contaminants is a serious and persistent problem and that (b) it can directly affect seals by inhibiting reproduction. Providing proof of this link for small cetaceans in the field is difficult, but achievable given carefully organised data collection and full consideration of possible confounding factors. In quantifying the time course of the bioaccumulation of POPs, it will be necessary to take account factors such as the general health, age and reproductive history and of each animal (work-packages 2 - 5).

The analysis encompasses the PCBs and p,p’-DDE as representatives of the ‘classical’ organohalogen compounds which probably cause a major part of the observed toxic effects as well as the relatively ‘new’ brominated flame retardants (PBDEs). Measurements from foetuses, neonates and milk of females of different ages will allow estimation of the transfer of pollutants from breeding females to their offspring and its relationships with age, contaminant load and health.

8. MEASUREMENT OF TOXIC ELEMENT LEVELS IN CETACEAN AND PREY TISSUES – leader UNILR (Florence Caurant)

Although not definitively linked with reproduction, the toxic elements represent important additional (possibly confounding) factors, to be considered when describing and modelling the relationship between POPs and reproduction. Little detail is known about relationships between metals and marine mammal physiology, disease or population dynamics (O’Shea, 1999). Liver and kidney samples from cetaceans, as well as samples from prey organisms (exposure assessment), milk and blood will be analysed for cadmium, mercury, methyl mercury and selenium.

9. SYNTHESIS AND MODELLING – leader UNIABDN (Graham Pierce)

Results will be synthesised to identify contaminants, geographic areas, cetacean populations, and prey species associated with negative impacts on reproduction and potential risks to cetacean population status. Recommendations will include identification of areas and issues of concern for the conservation of small cetaceans and management of pollution in coastal zone and open ocean waters. Quantitative results will be compared between areas, using appropriate statistical tests, and used to formulate simple empirical models. Several types and levels of model are needed, including quantitative descriptions of the effects of bioaccumulation for individuals and populations of each cetacean species. More detailed models should be possible for harbour porpoises and common dolphins, for which sample sizes are expected to be highest.

 

Partners

1. University of Aberdeen (UNIABDN): Graham Pierce, Begoña Santos, Jennifer Learmonth

 

2. Nationaal Natuurhistorisch Museum of Leiden (NNM): Marjan Addink, Chris Smeenk, Manuel Garcia Hartmann

 

3. Netherlands Institute for Sea Research (NIOZ): Jan Boon, Bart Zegers, Anchelique Mets

 

4. University of La Rochelle (ULR): Florence Caurant, Vincent Ridoux, Paco Bustamente, Laureline Meynier

 

5. Instituto de Investigaciones Marinas (IIM): Angel Guerra, Angel González, Camino Gestal

Subcontractor - CEMMA (voluntary strandings network): Alfredo López, Josep M. Alonso Farré

 

6. University College Cork (UCC): Emer Rogan, Sinead Murphy

 

7. Centre de Recherche sur les Mammifères Marins (CRMM): Willy Dabin, Olivier Van Canneyt

 

 

Collaborations

UK: Samples and data for strandings in Scotland were provided, under a collaboration agreement with the UK government-funded strandings network, by Scottish Agricultural College’s Veterinary Science Division. The UK strandings project is headed by Paul Jepson. Staff at SAC were Tony Patterson and Bob Reid. Contaminants analysis for UK samples was carried out by Robin Law at CEFAS. The collaboration agreement envisaged data sharing and joint publications. Additionally, Christina Lockyer (Age Dynamics) has participated in age determination workshops.

Netherlands: NNM collaborates with staff from the University of Liege (Jean-Marie Bouquegnau, Thierry Jauniaux) and the Free University of Brussels (Claude Joiris, Ludo Holsbeek). Under this agreement, samples from Dutch and Belgian strandings were pooled, with results leading to joint publications. Thierry Jauniaux was also involved in assisting with work under WP2 (necropsy) and WP3 (histopathology) at NNM

Data collection in France, Spain and Ireland wass carried out in association with local strandings networks. Other collaborations included provision of tissue samples for a genetic study of population structure in harbour porpoises.

 

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