Which are the main threats affecting the marine megafauna in the Bay of Biscay?
Introduction
The marine environment faces an increasing number of threats that are causing growing impacts on marine species and processes; with over a third of the world's oceans estimated to suffer high or very high impacts (Halpern et al., 2008). These threats are mostly driven by anthropogenic activities, such as overexploitation of marine resources, pollution and habitat degradation and destruction (Dulvy et al., 2003; Halpern et al., 2007; IPBES, 2019). In addition, climate change-driven processes such as extreme weather events, increasing temperature and acidification are having serious effects on marine habitats (Descamps et al., 2015; Harley et al., 2006; Vaughan et al., 2001). These threats could have a cumulative effect and therefore the assessment of their spatio-temporal patterns could be of crucial importance (Halpern et al., 2015; Maxwell et al., 2013). In a recent assessment (IPBES, 2019), over 40% of marine ecosystems were highly impacted by climate-driven anthropogenic threats and 66% experienced cumulative impacts.
In Europe, the Marine Strategy Framework Directive (MSFD; 2008/56/EC) aims to provide the legal framework to achieve the sustainable use of marine goods and services of European waters by effectively managing human activities and pressures through an ecosystem-based approach. The MSFD requires Member States (MS) to follow a series of steps with the aim of achieving (or maintaining) Good Environmental Status (GES) of their waters by 2020 (see Santos & Pierce, 2015). One of the requirements of the Directive is that MS should define what GES means for their waters, in terms of the eleven qualitative descriptors provided. The Directive defines that GES will be reached when “the overall state of the environment in marine waters provides ecologically diverse and dynamic oceans and seas which are healthy and productive”. MS are also required to set environmental targets and develop criteria (with associated thresholds) to reach GES, and to monitor the progress towards GES. The first descriptor of Biodiversity states that GES will be achieved when “Biological diversity is maintained. The quality and occurrence of habitats and the distribution and abundance of species are in line with prevailing physiographic, geographic and climatic conditions”. For this descriptor, the guidance provided by the European Commission (Cochrane et al., 2010) suggests a focus at the level of “functional group” (defined as “an ecologically relevant set of species”) for assessment and reporting. Highly mobile groups of species such as cetaceans and seabirds are included as two of these functional groups. Cetaceans and seabirds (‘marine megafauna’ hereafter) have key roles in marine ecosystem functioning, with changes in their abundance and distribution impacting ecosystem structure, function and resilience (Baum and Worm, 2009; Estes et al., 2011).
The Bay of Biscay (‘BoB’ hereafter) hosts numerous seabird and cetaceans species of high conservation value. In the case of seabirds, many species breed in Northern Europe, but spend the non-breeding period in this area (Pettex et al., 2017). Among seabirds, there are species classified as “Critically Endangered” (Balearic shearwater Puffinus mauretanicus), “Endangered” (Atlantic puffin Fratercula arctica), “Vulnerable” (black-legged Kkittiwake Rissa tridactyla) and “Near threatened” (razorbill Alca torda) (IUCN, 2018). Of the common cetacean species, the fin whale Balaenoptera physalus is classified as “Near threatened” and both the sperm whale Physeter macrocephalus and the harbour porpoise Phocoena phocoena as “Vulnerable” in Europe (IUCN, 2018). At the Spanish level, ten cetacean and four seabird species are listed as “Threatened” in the Royal Decree for the Development of the List of Wild Species in Regime of Special Protection and the Spanish Catalogue of Endangered Species (RD139/2011).
There is an overall lack of knowledge on the severity of the impact of different threats (e.g. climate change, pollution, fishing, habitat-related changes) on seabirds and cetaceans in the BoB. This information is valuable in the context of the MSFD to develop criteria and their associated thresholds to determine if GES is reached. Within this context, we provided the first assessment of the impact of different threats on the marine megafauna community of the BoB based on two complementary approaches. Firstly, we evaluated the quantitative information gathered for seabirds at Wildlife Rehabilitation Centres (WRCs) to provide the basis for an initial assessment. Secondly, we carried out a literature review to (1) identify the main threats affecting both seabird and cetacean species occurring in the BoB and (2) evaluate their potential impact on both taxonomic groups. Both approaches were compared to provide a full assessment of their potential impact on the marine megafauna in the BoB.
Section snippets
Selection of species
The species considered were those listed as present in the North Atlantic sub-region of the Spanish initial evaluation document for the MSFD (MAGRAMA, 2012a, 2012b). The conservation status of the species listed was obtained at the global, European and national level. For global and European level, we used the International Union for the Conservation Nature criteria (IUCN; www.iucn.org) and checked whether the species was listed in the Annex I of the Birds Directive (BD; Council Directive
Overall description
Data from a total of 4,023 admissions were available divided between WRCs as follows:: 1,616 (40.2%; 2014–2016 period) from the Gipuzkoa WRC, 1,854 (46.1%; 2014–2016 period) from the Bizkaia WRC, 227 (5.6%; 2010–2016 period) from the Cantabria WRC and 326 (8.1%; 2009–2016 period) from the Asturias WRC. The admissions included 29 species belonging to nine families (see Fig. 3a): Alcidae (41.2% of the total number of admissions), Laridae (38.9%), Sulidae (13.3%), Phalacrocoracidae (3.7%),
Discussion
The lack of knowledge on the impact that different threats could have on seabird and cetacean individuals and populations hampers the development of suitable mitigation measures despite the efforts of several expert groups in summarising the existing evidence and categorising these threats. The present study advances our knowledge on the main threats faced by the marine megafauna community in the BoB by providing new (quantitative) evidence of their impact on seabird species (based on WRCs
Conclusions
The marine megafauna of the BoB faces several threats with species scoring differently under different threats depending on their biology and habitat use. The information collected and summarised in the present work can help identify conservation priorities (combination of threats and species requiring the most urgent management measures), work needed in the context of MSFD and other relevant legislation. Our complementary assessment is of special relevance for threatened species inhabiting the
Acknowledgements
Thank you to the General Directorate of the Natural Environment of the Government of Cantabria, General Directorate of Natural Resources of the Government of Asturias, Department of Sustainability and Natural Environment of the Provincial Council of Bizkaia and Department of Economic Promotion, Rural Environment and Territorial Balance of the Provincial Council of Gipuzkoa for facilitating the data of the WRCs to perform this study. We also thank to all the staff of the WRCs. IGB was funded by
References (89)
- et al.
The Gray Zone: relationships between habitat loss and marine diversity and their applications in conservation
J. Exp. Mar. Biol. Ecol.
(2008) - et al.
Current global risks to marine mammals: taking stock of the threats
Biol. Conserv.
(2018) - et al.
Potential risk of harmful algae transport by ballast waters: The case of Bilbao Harbour
Mar. Pollut. Bull.
(2011) - et al.
The impact of introduced predators, light-induced mortality of fledglings and poaching on the dynamics of the Cory's shearwater (Calonectris diomedea) population from the Azores, northeastern subtropical Atlantic
Biol. Conserv.
(2011) - et al.
Incidence of plastic ingestion in seabirds from the Bay of Biscay (southwestern Europe)
Mar. Pollut. Bull.
(2019) - et al.
The impact of debris on marine life
Mar. Pollut. Bull.
(2015) - et al.
Climate change and marine plankton
Trends Ecol. Evol.
(2005) - et al.
Analysis and quantification of microplastics in the stomachs of common dolphin (Delphinus delphis) stranded on the Galician coasts (NW Spain)
- et al.
Threshold responses in bird mortality driven by extreme wind events
Ecol. Indicat.
(2019) - et al.
Light-induced bird strikes on vessels in Southwest Greenland
Mar. Pollut. Bull.
(2011)
Small cetacean bycatch as estimated from stranding schemes: the common dolphin case in the northeast Atlantic
Environ. Sci. Policy
The contribution of stranding data to monitoring and conservation strategies for cetaceans: developing spatially explicit mortality indicators for common dolphins (Delphinus delphis) in the eastern North-Atlantic
Ecol. Indicat.
Using large scale surveys to investigate seasonal variations in seabird distribution and abundance. Part II: the Bay of Biscay and the English Channel
Deep Sea Res.
Incidence of entanglements with marine debris by northern gannets (Morus bassanus) in the non-breeding grounds
Mar. Pollut. Bull.
Biomagnification of persistent organic pollutants in a deep-sea, temperate food web
Sci. Total Environ. 605–
A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs
Mar. Pollut. Bull.
Impacts of oil spills on seabirds: unsustainable impacts of non-renewable energy
Int. J. Hydrogen Energy
The incidental catch of seabirds in gillnet fisheries: a global review
Biol. Conserv.
Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management
Ann. Rev. Mar. Sci.
Foraging distances of a resident yellow-legged gull (Larus michahellis) population in relation to refuse management on a local scale
Eur. J. Wildl. Res.
First-year movements of yellow-legged gull (Larus michahellis Lusitanius) from the southeastern Bay of Biscay
Waterbirds
Cascading top-down effects of changing oceanic predator abundances
J. Anim. Ecol.
Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia
Evidence for ship noise impacts on humpback whale foraging behaviour
Biol. Lett.
Libro Rojo de los Vertebrados de España
Implications of a zoned fishery management system for marine benthic communities
J. Appl. Ecol.
Marine mammal welfare: behaviour judge ambiguous cues more optimistically
Increasing frequency of extreme El Niño events due to greenhouse warming
Nat. Clim. Chang.
Reducing the conflict between cormorantsand fisheries on a pan-european scale: REDCAFE - summary and national overviews
Marine Strategy Framework Guidance on the Interpretation and Application of Descriptor 1: Biological Diversity
Seabird conservation status, threats and priority actions: a global assessment
Bird. Conserv. Int.
Demographic effects of extreme weather events: snow storms, breeding success, and population growth rate in a long-lived Antarctic seabird
Ecol. Evol.
Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH
Estuar. Coasts
Extinction vulnerability in marine populations
Fish Fish.
Impact of climate change on marine pelagic phenology and trophic mismatch
Nature
Trophic downgrading of planet earth
Science
Conservation of cetaceans
The effect of weather conditions on the feeding behaviour of a diving bird, the common guillemot Uria aalge
J. Avian Biol.
Thermodynamic modelling predicts energetic bottleneck for seabirds wintering in the northwest Atlantic
J. Exp. Biol.
A critical evaluation of the Bay of Biscay as a candidate for a Marine Protected Area
Cetacean occurrence, habitat preferences and potential for cetacean-fishery interactions in Iberian Atlantic waters: results from cooperative research involving local stakeholders
Aquat. Conserv. Mar. Freshw. Ecosyst.
A systematic review on the behavioural responses of wild marine mammals to noise: the disparity between science and policy
Can. J. Zool.
Rapid biogeographical plankton shifts in the north atlantic ocean
Glob. Chang. Biol.
Spatial and temporal changes in cumulative human impacts on the world's ocean
Nat. Commun.
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2020, Marine PolicyCitation Excerpt :Although there is high growth expectation, there are current environmental concerns in the area. Increasing shipping density brings higher likelihood of strikes (particularly affecting baleen whales and large odontocetes such as sperm and fin whales) [11]. Besides, shipping is seen as the reason of a growing threat of the introduction of non-indigenous species through ballast waters which can in turn transmit new pathogens to the indigenous species of the bay.
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2020, Ecological IndicatorsCitation Excerpt :It highlights the importance of long-term monitoring to measure changes through time, assisting scientists, managers and policy makers to forecast and prepare for a possible redistribution of species due to climate change or other pressures, with ecological, social and economic consequences (Miloslavich et al., 2018). In addition, the identification of HVBAs is crucial to identify where conservation efforts are required, to assist with the allocation of resources (García-Barón et al., 2019; Lambert et al., 2017b). HVBAs may help to identify new potential marine protected areas or quantify gaps in the current network of protected areas (e.g. Natura 2000 network).
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2020, Marine Environmental ResearchCitation Excerpt :Most studies carried out in European waters focused on studying the use of discards by seabirds in breeding areas such as the North Sea or the Western Mediterranean (Arcos and Oro, 2002; Camphuysen, 1995; Garthe, 1997; Martinez-Abrain et al., 2002; Tyson et al., 2015). However, the Bay of Biscay is an important migratory flyway as most breeding seabirds in northern Europe cross this biogeographical area during their annual migrations, while represents a wintering area for certain individuals, populations or species (Brereton et al., 2003; García-Barón et al., 2019; Pettex et al., 2017). A reflection of this is that during winter months and pre-breeding migration (December–April) the number of birds per fishing operation was higher.