THE DIET OF HARBOUR PORPOISES (PHOCOENA PHOCOENA) IN THE SOUTHERN NORTH SEA: A RELATIONSHIP WITH PREY AVAILABILITY

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Protection status of harbour porpoises in the European waters

In the European waters, the status of harbour porpoises has been of concern for many years. Conservation measures in form of several international, European and national (French) conventions and regulations were implemented in order to protect the harbour porpoise. At the international level, the Bern convention (1979) aims to conserve wild flora and fauna and their natural habitats and also aims to promote European cooperation in order to protect migratory species. In addition, the harbour porpoise figures on the IUCN (International Union for Conservation of Nature) red list of threatened species. Moreover, the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) cited cetaceans as protected species against over-exploitation through international trade. At the European level, the ASCOBANS (Agreement on the Conservation of Small Cetaceans of the Baltic, North East Atlantic, Irish and North Seas) conservation plan obliges signatories to apply the conservation, research and management measures prescribed in the annex. Those involve bycatch reduction, pollution control, research and monitoring. The Habitat Directive (92/43/EEC) list harbour porpoise in annex II and IV, which means that favorable conservation status of this species has to be achieved and Special Areas of Conservation (SACs) are to be designated for this species where needed. The European regulation (812/2004) determines the measures to take concerning incidental catches of cetaceans and aims to reduce by-catch in some fisheries. Finally at the national level, this species figures in the French Decree of 27 July 1995 and the Decree of 9 July 1999 as protected endangered species. Moreover, the Oceans Round Table (Grenelle de la Mer 2009) has advised in the article 14.f to strengthen measures to protect/restore threatened marine species and/or marine sanctuaries and mammals by helping to create new sanctuaries and has also advised in the article 16.b to take the necessary measures to limit noise pollution, collisions with ships and incidental catches in fishing gear.
Figure 1.4 Predicted density surface for harbour porpoises in 1994 (SCANS survey, figure on the left) and in 2005 (SCANS II survey, figure on the right); the color bar indicates porpoises density (number of animals per km2) (Hammond et al., 2013).

Diet of harbour porpoises

The diet arising from stomach content analysis for about 100 harbour porpoises stranded between 1989 and 1994 along the UK waters consisted mainly on gadoids, sandeels and gobies (Martin, 1996). In Scottish waters, about 188 stomachs investigated for porpoises stranded between 1992 and 2003 mainly included whiting, sandeels and gadoids such as Trisopterus sp. (Santos et al., 2004). In 2006, stomach contents of 64 porpoises stranded along the Dutch waters mainly included gobies, sandeels, sprat, herring, whiting and twait shad (Leopold and Camphuysen, 2006). A more recent study on 64 porpoises stranded between 1997 and 2011 along the Belgian waters showed that porpoise’s stomachs mainly included gobies, sandeels and gadoids such as whiting and Trisopterus sp. (Haelters et al., 2012). More studies on the diet of harbour porpoises are presented in table 1.1.
The North Sea is a large, semi-enclosed, epi-continental sea with a relatively shallow mean depth of 90 m with deeper areas in the north of the Norwegian Trench (700 m) (Ducrotoy et al., 2000) and surrounded by large and highly developed societies (Ducrotoy and Elliott, 2008). This area is subject to several anthropogenic activities such as fishing pressures and coastal industrial activities (artisanal and industrial use of the coast). It supports large-scale commercial fishing and is an example of a region where fishing has substantially impacted forage fish populations (Dickey-Collas et al., 2014). The North Sea is regarded as a moderately polluted sea area where the input and transport of contaminants have been discussed in previous studies (Anderson et al., 1996; OSPAR, 2010). It is a productive and biologically rich area, and therefore it sustains numerous marine mammals. Most marine mammals depend on an abundant supply of local food; for that reason fishing may negatively affect their survival by reducing the availability of prey or by inducing its dispersal (Lassalle et al., 2012). The depletion of fish stocks is a result of serial demand on fish protein explained by overfishing (Read et al., 2006). Major changes in the North Sea food web are taking place which might introduce changes in marine mammals feeding habits. The decrease of sandeel and the increase of sprat along with the lower energy value of both species in the diet were linked to breeding failure of seabirds in the North Sea in 2004 (Wanless et al., 2005). A lack of sandeel consumption was linked to an increased starvation in harbour porpoises in the Scottish North Sea (MacLeod et al., 2007). These authors suggested that the decrease of the sandeel availability in response to climate change may have negative effects on habrour porpoises population in the North Sea by increasing the starvation in spring.
Overall on the French coasts in the Channel and the southern North Sea, the Atlantic and the Mediterranean, 11 species of cetaceans have been recorded in the stranding in the year 2013. Among these species, the harbour porpoise is for the first year (for more than 40 years of monitoring in France) the most represented species in the strandings with 43.7 % just before the common dolphin (Delphinus delphis) with 42.4 %. Moreover, among the 6 species found in the English Channel and the southern North Sea (along the French coast) in 2013, the harbour porpoise was predominant in the composition of stranding with more than 90% of the total stranded animals (Figure 1.5) (Van Canneyt et al., 2014).
Figure 1.5 Species composition (%) of stranded cetaceans along the English Channel and the North Sea (French coast) in 2013. Sowerby’s beaked whale Mesoplodon bidens, long-finned pilot whale Globicephala melas, Risso’s dolphin Grampus griseus, Common bottlenose dolphin Tursiops truncatus, Short-beaked common dolphin Delphinus delphis and Harbour porpoise Phocoena phocoena; n = 368 (Van Canneyt et al., 2014).
More specifically, over the past decade harbour porpoises stranding has increased in the southern North Sea particularly in the French, Belgian and Dutch coastal waters (Camphuysen et al., 2008; Haelters and Camphuysen, 2009; Van Canneyt et al., 2014). According to the stranding data in the Channel and the North Sea (French coast), an increase in the number of stranded animals from the late 90s onwards was found (Figure 1.6a). Only a few animals were stranded between 1990 and 1998 (maximum 9 individuals per year with a total of 29 animals stranded in 9 years). This number increased to more than 58 stranded individuals per year in the period 2004-2011 with a maximum of 94 individuals stranded in 2007. In the year 2012, the number of stranded porpoises (186 animals) was almost the double of the previous year (90 stranded animals in 2011). The same trend was observed in 2013 with almost the double of porpoises stranded (333 animals) compared to the previous year 2012. Alongside, in the southern North Sea on the Belgian coast similar trends of stranding occurred in the past few decades. As shown in the figure 1.6b, an increase in the number of stranded animals from the late 90s onwards was found. Only a few animals were stranded between 1990 and 1997 (maximum 6 individuals per year). This number increased to more than 85 stranded individuals per year in the period 2005-2007. In 2008 and 2009 the increase was interrupted, with respectively 62 and 66 stranded individuals per year. In 2011, the stranding of porpoises increased again.
Figure 1.6 Annual distribution of stranded harbour porpoises in (a) the English Channel and the North Sea (French coast) between 1990 and 2013 (Van Canneyt et al., 2014), (b) the southern North Sea on the Belgian coast between 1990 and 2012 (T. Jauniaux personal communication) and (c) the French Atlantic coast between 1990 and 2013 (Van Canneyt et al., 2014).
The increase in stranding harbour porpoises has also been observed in Dutch waters between 1998 and 2007. A minimum of 59 stranded individuals in 1998 and a maximum of 539 individuals in 2006 were recorded (Camphuysen et al., 2008). Similarly on the French Atlantic coast (Bay of Biscay) since the late 1990s, the increase of stranded porpoises has been observed reaching a maximum of 164 stranded individuals in 2013 (Figure 1.6c) (Van Canneyt et al., 2014). Stranding data seems to indicate that the stranded individuals are mainly composed of juveniles with significantly more males than females. The increase in number of stranded porpoises in Belgian and Dutch coastal waters consisted mainly of juveniles (Haelters and Camphuysen, 2009). Distinct peaks of stranding were remarkable between March and May for the French coast in the southern North Sea and between December and January for the Atlantic French coast. This increase in numbers of stranded porpoises was believed to be probably an anomaly of abundance and/or particular mortalities in the French waters (Van Canneyt et al., 2014). As for the Belgian and Dutch coasts, distinct peaks were remarkable between March and May followed by another peak in August. This increase in numbers of stranded porpoises in the southern North Sea is probably food related and is believed to be due to an influx of animals from more northern waters (Haelters and Camphuysen, 2009; Hammond et al., 2013).
Harbour porpoises in the North Sea are very sensitive to anthropogenic disturbances and the main threats on their distribution/abundance may be represented by the interaction with different human activities. Despite all the conventions and regulations, this species is still exposed to several potential threats due to human impacts. The major threats are the incidental catches in fishing gears (bycatch), the contaminant exposure and the depletion of favorite, nutritive rich prey species through overfishing (Reijnders, 1992; Bennett et al., 2001; Herr et al., 2009; Bjørge et al., 2013). However, other anthropogenic disturbances such as noise pollution caused by sonar and climate change might also threaten porpoise’s status.
• The bycatch in fisheries is the main direct threat to small cetaceans in the European Atlantic waters (ICES, 2013a). Monitoring programs of Danish set-net fisheries in the North Sea revealed an average of 5 591 porpoises taken annually in the period 1987-2001 in the center and southern North Sea (Vinther and Larsen, 2004). In addition, by-catch in coastal gill net fisheries in Norway was estimated at more than 20 500 porpoises during 2006-2008 (Bjørge et al., 2013). According to the management objectives defined by ASCOBANS this annual by-catch is not sustainable. Moreover, from 43 stranded porpoises investigated along the Belgian coast, 11 specimens were suspected to have been caught incidentally in fishing gear (ICES, 2013a). A threshold of 1.7% of the best estimate of population abundance should not be exceeded for annual by-catch. Unfortunately, no specific monitoring programs for marine mammal’s by-catch took place in most countries of the North Sea (ICES, 2013a).
• The contaminant exposure is a potential threat for the harbour porpoises in the North Sea. This species is known to inhabit coastal waters close to pollution sources. This long-lived species feeds at a high trophic level, thus it can accumulate relatively high levels of contaminants. Several studies have been interested in the study of chemical contaminants in harbour porpoises from the North Sea (Jepson et al., 1999; Siebert et al., 1999; Bennett et al., 2001; Das et al., 2004b).
• The overfishing can lead to a decline of favored, nutritive rich prey species for porpoises. This can have an impact on their diet composition and their abundance and/or distribution. Harbour porpoises are small cetaceans with limited body fat and energy storage capacity; therefore, they must feed at a high daily rate without prolonged periods of fasting to maintain energy requirements (Koopman et al., 2002). Hence, this species is highly sensitive to changes in food availability for instance caused by overfishing and/or other changes in environmental conditions (Read and Hohn, 1995). Many fish species consumed by harbour porpoises have commercial value and are highly exploited. A shift in the diet of porpoises has been witnessed after the collapse of the herring stock in the southern North Sea (Santos and Pierce, 2003).
• The noise pollution such as construction of offshore wind farms (Haelters, 2009), shipping, military activities, etc may have direct effects on individuals. Harbour porpoises use sound for navigation, finding food and communication and are therefore sensitive to acoustic pollution. The harbour porpoise mass stranding in Danish waters in 2005 was partly related to the military activity in the region (Wright et al., 2013).
• Climate change may act on harbour porpoise population in different ways. Indirect effects of climate change include changes in prey availability affecting distribution, abundance and migration patterns, community structure, susceptibility to disease and contaminants (Learmonth et al., 2006; Hammond et al., 2013). For instance, the sandeel availability in response to climate change may have negative effects on habrour porpoises population in the North Sea by increasing the starvation in spring. In fact, an increased starvation in harbour porpoises in the Scottish North Sea was linked to a lack of sandeel consumption (MacLeod et al., 2007).

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Assessment of chemical contamination

A potential threat for marine mammals in response to human activities is represented by the contaminant exposure (Bjørge, 2003). The contaminant load in the tissues and organs of dead or washed ashore marine mammals might provide a useful indicator of certain pollutants in coastal marine ecosystems. However, a healthy or unhealthy ecosystem might not be directly related to the robust or declining marine mammals stock (Mangel and Hofman, 1999). Marine mammals are top predators and consequently, they tend to accumulate relatively high levels of contaminants (Duinker et al., 1989; Tanabe et al., 1994). Hence, the toxic effects of contaminants on vulnerable animals such as cetaceans should be considered from an ecotoxicological perspective (Tanabe et al., 1994; Kleivane et al., 1995).
Metals are encountered in the environment as a result of both human activities and natural processes. Some of these metals such as Cu, Cr, Mn, Se and Zn are essential for effective immune functioning, while others such as As, Cd, Hg, Pb and V are non essential elements and therefore leading to autoimmune diseases (Lynes et al., 2006). Uptake from water and food (trophic transfer) are several sources contributing to metal accumulation in marine animals (Wang and Rainbow, 2010). Essential trace elements are slightly variable from animal to animal, whereas the potential toxic elements are much greater variable with concentration ranges often covering several orders of magnitude (Mackey et al., 1995). High levels of metal contaminants have been documented in various studies on marine mammals. These studies suggested that metal contaminants may have immunological effects on marine mammal’s health. For instance, the exposition of seals to high Zn concentrations in Caspian Sea resulted in the disturbance of homeostatic control and nutritional status of essential elements (Anan et al., 2002). Moreover, correlations between severities of disease and liver Hg levels were detected in harbour porpoises from the German waters (Siebert et al., 1999). Metals have been shown to produce alteration in the immune function of harbour seals from the Antarctic, which may decrease resistance to infectious diseases encountered by marine mammals (Frouin et al., 2010). High Zn concentrations in harbour porpoises form UK that died of infectious disease may represent a response to infection and other stressors (like cold) causing Zn redistribution (Bennett et al., 2001). Moreover, porpoises from the North Sea displaying lesions of the respiratory tract had higher hepatic Zn burden than porpoises without lung lesions (Das et al., 2004b). In addition, Lahaye et al., (2007) suggested that different biological and ecological factors might be related to trace element levels in harbour porpoises, which can explain the significant geographical differences in hepatic Zn concentrations. Moreover, the elevated Cd levels obtained in Scottish porpoises could be related to their feeding preferences. A study on five toothed whales from the Northwest Iberian Peninsula revealed that differences in metallic concentrations are probably related to biological factors such as age and sex and/or to ecological factors such as feeding habits or bioavailability of the various elements. Pilot whales and striped dolphins showed the highest concentrations of Cd and Hg compared to harbour porpoise, common dolphin and bottlenose dolphin (Méndez-Fernandez et al., 2014b). Along the North Sea, harbour porpoises form England and Whales, northern France, Belgian and German coasts tend to accumulate some metals according to their health status (Siebert et al., 1999; Bennett et al., 2001; Das et al., 2004b). Table 1.2 represents an overview of some metal levels in organs of harbour porpoises stranded between 1990 and 2004 in different areas of the North Sea and adjacent waters.

Table of contents :

CHAPTER 1 INTRODUCTION
The harbour porpoise (Phocoena phocoena)
Distribution and description
Distribution on a local scale
Protection status of harbour porpoises in the European waters
Diet of harbour porpoises
Threats
Assessment of chemical contamination
Studying the feeding ecology of harbour porpoises
Objectives of the study
Outline of the study
CHAPTER 2 STRATEGIES, PROTOCOLS AND METHODOLOGIES
1. Sample collection and necropsies
1.1. Carcasses collection
1.2. Protocol of dissection, collection and preservation of samples
2. Chemical analyses
2.1. Metallic analyses
2.1.1. Analysis on ICP-AES
2.1.2. Analysis on ICP-MS
2.1.3. Analysis on AMA-254
2.1.4. Quality control procedures
2.2. Persistent Organic Pollutants analyses
2.3. Data treatment
3. Feeding ecology
3.1. Stomach content analysis
3.1.1. Otoliths
3.1.2. Diet composition
3.1.3. Feeding strategy
3.2. Stable isotopes analysis
3.3. Fatty acids analysis
3.4. Compound-Specific Stable Isotope Analysis (CSIA)
3.5. Data treatment
3.5.1. Mixing model: Stable isotope analysis in R (SIAR)
3.5.2. Fatty acids data treatment
3.6. Environmental data
CHAPTER 3 HARBOUR PORPOISES (PHOCOENA PHOCOENA) STRANDED ALONG THE SOUTHERN NORTH SEA: AN ASSESSEMENT THROUGH METALLIC CONTAMINATION
Abstract
Introduction
1. Materials and methods
1.1. Sampling and data collection
1.2. Metal analysis
1.3. Data treatment
2. Results
2.1. Metal contaminants and maturity status
2.2. Metal contaminants and causes of death
3. Discussion
3.1. Non essential elements
3.2. Essential elements
3.3. Temporal trends
Conclusion
Acknowledgements
CHAPTER 4 ORGANOCHLORINES IN HARBOUR PORPOISES (PHOCOENA PHOCOENA) STRANDED ALONG THE SOUTHERN NORTH SEA BETWEEN 2010-2013
Abstract
Introduction
1. Materials and methods
1.1. Sampling and data collection
1.2. POP analysis
1.3. Data treatment
2. POP results
2.1. POPs and maturity status
2.2. POPs and causes of death
3. Discussion
3.1. PCB levels
3.2. DDX levels
Conclusion
Acknowledgements
CHAPTER 5 THE DIET OF HARBOUR PORPOISES (PHOCOENA PHOCOENA) IN THE SOUTHERN NORTH SEA: A RELATIONSHIP WITH PREY AVAILABILITY
Abstract
Introduction
1. Materials and methods
1.1. Sampling and data collection
1.2. Stomach content analyses
1.3. Stable isotopes analyses
1.4. Fatty acids composition
1.5. Compound-Specific Stable Isotope Analysis (CSIA)
1.5. Data treatment
2. Results
2.1. Stomach contents
2.2. Stable isotopes and SIAR
2.3. Fatty acids composition and CSIA
3. Discussion
3.1. Diet of harbour porpoises stranded along the southern North Sea
3.2. General diet composition
Conclusion
Acknowledgements
CHAPTER 6 FEEDING HABITS OF HARBOUR PORPOISES (PHOCOENA PHOCOENA) FROM THE SOUTHERN NORTH SEA AND THE BAY OF BISCAY INFERRED FROM A MULTI APPROACH DIETARY ANALYSES
Abstract
Introduction
1. Materials and methods
1.1. Sampling and data collection
1.2. Stomach content analysis
1.3. Stable isotopes analysis
1.4. Fatty acids analysis
1.5. Data treatment
2. Results
2.1. Stomach contents
2.2. Stable isotope analyses of δ13C and δ15N
2.3. Lipid composition
3. Discussion
3.1. Diet composition
3.2. Comparison with previous studies
Conclusion
Acknowledgements
CHAPTER 7 GENERAL DISCUSSION
Contamination status of harbour porpoises in the southern North Sea
Changes in the distribution of harbour porpoises in the North Sea
Value of a multi-approach dietary analysis
Conclusions and perspectives
REFERENCES

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