Learn about the climate emergency, the causes and what to do about it

Climate change and the decline of seabirds

Seabirds are sensitive to alterations in the environment (Parsons et al., 2008, Irons et al., 2008). Climate change affects them directly due to the impact of bad weather and indirectly by reducing their food supply and increasing predation and parasitism (Frederiksen et al., 2008; Oswald et al., 2011, Gaston, A.J. and Elliott, K.H., 2013). Globally their numbers are falling dramatically; the scale of decline has recently been established (Paleczny et al., 2015). It appears that such reductions in seabird numbers could indicate a marine wildlife catastrophe.

Human activities and natural events have exacerbated the recent sudden increase in global temperatures (Reid et al., 2016; Goberville, E., Beaugrand, G. and Edwards, M., 2014). This has caused a rapid and abrupt reorganisation of the ecosystem known as a ‘regime shift’ - a tipping point difficult to reverse (Beaugrand et al., 2008; Barange et al., 2008, Russell et al., 2015, Reid et al, 2016, MacDonald et al., 2015). It is happening across the Northern Hemisphere, and probably globally as well (Beaugrand et al., 2015).

Dwindling seabirds is a phenomenon not confined to the north-east Atlantic. Approximately 230m or 69.7 per cent of the world’s monitored seabirds perished in the 60 years between 1950 and 2010. The monitored population is approximately 19 per cent of the global seabird population. On a global scale human activities are having a very strong impact on seabird population (Paleczny et al., 2015).

Seabirds are indicators of the health of marine ecosystems (Parsons et al., 2008) and therefore the deaths of so many suggest that a worldwide regime change has already occurred. This has been described (WWF, 2015) as “a crisis in global oceans as populations of marine species halve in size since 1970”. And as “disastrous for ecosystems and spells trouble the world over, especially for people in the developing world who depend heavily on the ocean’s resources”.

The underlying changes to the marine environment are complex but regime change is driven by climate change, human activities or, a combination of the two (Beaugrand et al., 2008). The deaths of such large numbers of seabirds represents an ecological disaster happening slowly, out of view and over many decades.

Studies provide evidence for the decline

Figure 1 shows the most recent abundance trends for Scotland and seabird species grouped by feeding and nesting preferences. The biggest declines are among the sandeel specialists and surface feeders. The Common Gull (Larus canus) is not shown in the table as species grouping data is unavailable. It was the only species to show a positive trend of nine per cent. Arctic tern (Sterna paradisaea) abundance may have been positively affected by a successful mink eradication programme on the Western Isles (Clode and MacDonald, 2002).

A recent study of the link between climate and bird populations in continental Europe and Britain provided the evidence that a regime change caused by warmer ocean temperatures is affecting the entire north-east Atlantic (Russell et al., 2015). Earlier papers identified three bioclimatic variables correlating with plankton abundance and sandeels, winter and spring sea surface temperature, rainfall (during the breeding season), and mean air temperature of the warmest month (Furness and Tasker, 2000; Thompson P. M., Ollason J. C., 2001; Frederiksen et al., 2006; Frederiksen et al., 2007; Irons et al., 2008; Oswald et al., 2011).

These factors were examined on a much larger scale than previous research. Using a technique called ‘bioclimate envelope modelling’ the north-east Atlantic was studied with three important results.

The first was obtained via use of a model that was created to predict the stability of the climate in smaller cells around the UK.  The predictions were examined to determine whether or not they correlated with population sizes. The result was that in half the species there was a significant relationship between suitability of climate for the species and how many animals were actually breeding.

The second result was obtained by checking whether those species that had a good relationship between the distribution in Europe and the climate also had a strong relationship between population size and the predicted climate suitability in the UK. The result was that those species that were more sensitive to changes in food availability were the ones most affected by climate. These species included those that cannot dive deeply (terns and kittiwakes) or those that return to the same site each year to breed - behaviour called breeding-site fidelity (puffins, razorbills and guillemots).

The third result was that those species that appeared most sensitive to climate variation were the ones that had decreased the most over the past 25 years. The spatial variation in climate affects the population of seabird species breeding in the UK and has already affected the species studied (Russell et al., 2015).

 

 

Figure 1 - Seabird Species Grouped by their feeding and nesting preferences with Abundance Trends for Scotland

 

Surface feeder

Sub-surface feeder

Sandeel specialist

Discard feeder

Inshore feeder

Offshore feeder

Cliff nester

Flat-ground nester

% Change in Abundance

Northern fulmar

X

 

 

X

 

X

X

*

-32

European shag

 

X

X

 

X

 

X

*

-54

Arctic skua

X

 

X

 

X

 

 

X

-82

Black-legged Kittiwake

X

 

X

 

 

X

X

 

-77

Sandwich tern

X

 

X

 

X

 

 

X

-60

Common tern

X

 

X

 

X

 

 

X

-21

Arctic tern

X

 

X

 

X

 

 

X

-44

Common guillemot

 

X

X

 

 

X

X

*

-21

Black guillemot

 

X

 

 

X

 

X

X

-33

Herring gull

X

 

 

X

X

X

X

X

-44

Great black-backed gull

X

 

 

X

X

X

X

X

-54

 

Sourced from SNH (2016a) and JNCC (2015)

*Although the Northern fulmar (Fulmarus glacialis), European shag (Phalacrocorax aristotelis) and Common guillemot (Uria aalge) are listed as predominantly cliff nesters on some sites they use flat ground for nesting.

 

Twenty-four species of seabird breed in Scotland; nearly a third of the European Union total. There are approximately 5m nesting seabirds in some of the largest seabird populations in Europe. For this reason, 50 special protection areas were created in Scotland and are monitored by experts and volunteers who count birds (see Figures 2 and 3). The resulting data-sets help scientists to predict population trends but the picture is complex. Some of the largest colonies in the northern isles Orkney and Shetland are declining, while in the south some of the sites are stable, while others are increasing (JNCC, 2015).

Figure 2: Special Protection Areas for Seabirds in Scotland

Sourced from SNH (2012).

 Scottish Natural Heritage (SNH) produce biodiversity indicators of the breeding numbers for 12 species and breeding success for 13. Surface feeders such as the kittiwake and terns are faring badly. The breeding failures of surface feeding seabirds has continued since 2003. The latest 2016 results based on data from 1986 to 2014 show that breeding success and breeding numbers have both declined since 1986 (see Figures 3 and 4). Breeding numbers are now 62 per cent of the 1986 level. Some kittiwake colonies have declined by more than 90 per cent. The northern strongholds of the kittiwake and Arctic skua have declined by more than 90 per cent in some cases. In Orkney, many of the cliffs that supported flourishing noisy colonies of kittiwakes are almost empty. The kittiwake decline in the North Atlantic Ocean has been severe and looks set to continue. The Arctic skua, which nests on the northern isles and robs other seabirds of their sandeels, is now rare. The European shag, kittiwake, and puffin have been added to the International Union for Conservation of Nature (IUCN) Red List of threatened birds because of serious declines in UK breeding populations. The puffin has also been red-listed due to rapid population decline across its European range (Furness, 2010; MacDonald et al., 2013; SNH, 2014; SNH, 2016a; JNCC, 2015; Eaton et al., 2015; SNH, 2016b).

 Figure 3: Index of breeding numbers (abundance) of seabirds 1986 to 2018. Index set to 100 at start of period. Blue dashed line shows average index level from 2011 to 2018.

The above chart is sourced from Marine Scotland Assessment (MSA, 2021).

 Figure 4 - Index of breeding success of seabirds 1986 to 2018. Index set to 100 at start of period. Blue dashed line shows average productivity from 2011 to 2018.

The above chart is sourced from Marine Scotland Assessment (MSA, 2021).

 

The decline of a key species of plankton

Changes to the plankton fauna are having an effect on seabird populations.

The food web is a representation of ‘what eats what’ in an ecological community. At the base of all marine food chains is phytoplankton. These synthesise carbon into organic compounds (known as primary producers). Above them are zooplankton such as Calanus finmarchicus, which is a keystone-species. Keystone-species are those that the food-chain cannot do without to the extent that their removal can start a regime shift (Hays et al., 2005; Beaugrand et al., 2008; Barange et al., 2008, Heath et al., 2009).

In 1931 zoologist Sir Alister Hardy invented the Continuous Plankton Recorder (CPR) to monitor plankton in the north-east Atlantic. More than 80 years of data show the multiple effects from climate, the fishing industry, general pollution and other factors affect the plankton fauna. Scientists have used the data to prove that increased sea-surface temperatures in the North Sea are changing the plankton fauna (Russell, 2015).

The long-term data-sets show that there was a regime change 30 years ago indicated by the decline of Calanus finmarchicus. This fatty cold water species is failing to adapt to the warmer temperatures with a 70 per cent decline in abundance in the North and Irish Seas (Heath et al., 2009). It is being replaced by the warm water species Calanus helgolandicus (Heath et al., 2012, Hinder et al., 2014; Arnott and Ruxton, 2002).

These changes at the bottom of the food-web are affecting the ecology of the whole of the northern Atlantic - an enormous area (Edwards et al., 2011; Planque, B., and Batten, S.D., 2000).

The alterations to the plankton fauna have grave consequences for the species above them such as the sandeel. There are five species of these in the North Sea, the lesser sandeel (Ammodytes marinus)[1] being the most plentiful. It connects primary and zooplankton production with top predators such as seabirds and larger fish and thus it is a keystone-species of forage fish. The staple food for sandeels, Atlantic cod (Gadus morhua L.), and other fish is Calanus finmarchicus. When sea temperatures rise the numbers of sandeels during the egg and larval stages fall. This inversely proportional relationship is linked to the abundance of Calanus finmarchicus at the time of egg sandeel hatching. Due to the decline of Calanus finmarchicus sandeels must now rely on a less nutritious species such as Calanus helgolandicus. Researchers used CPR data to show that rising temperatures since the mid-1980s have modified the plankton ecosystem in a way that reduces the survival of young cod (Beaugrand et al., 2003; Lanchbery, J., 2006).

Because long-term data-sets from CPR monitoring programmes exist for the north-east Atlantic the effects of interactions between plankton and marine ecosystems have been studied. Elsewhere scientists lack the data to determine whether declines in key species of plankton might be causing a regime change.

The sandeel population is threatened

Even if the plankton were not declining, the sandeel would still be at risk in the UK because it cannot adapt to warmer sea temperatures. Its larvae hatch out later and this leads to poorer growth rates and reduced weight and length. Additionally, warmer sea temperatures affect the survival rate of juvenile organisms. Sandeels are a burrowing species requiring a sandy sediment with low clay density for respiration. This close association with coarse sandy sediments prevents the species from moving to deeper waters as sea temperatures increase (Wright, P. J., and Bailey, M.C., 1996.; Wright, P. J., Jensen, H., and Tuck, I., 2000; Arnott and Ruxton, 2002; Edwards et al., 2011, Heath et al., 2012; Lancaster et al., 2015; Solomon et al., 2009).

Sandeels are energy-rich fish that breeding seabirds such as terns feed to their chicks. Seabird breeding productivity is reliant upon the body size or biomass of sandeels and these are declining. The Atlantic puffin (Fratercula arctica) and other species that have high breeding-site fidelity are particularly affected. Species such as the black-legged kittiwake[2] (Rissa tridactyla) and terns that hunt for fish that swim just below the sea surface also suffer (Frederiksen et al., 2005; Wanless et al., 2005; Frederiksen et al, 2006; Frederiksen et al., 2007; Furness, 2010; Engelhard et al., 2014, MacDonald et al., 2015). In the northern isles of Scotland some colonies of Kittiwakes have declined by over 90 per cent, and reduced sandeel population is the most likely cause (SNH 2016a).

The iconic puffin is regularly photographed with a beak full of sandeels, their staple diet. Now the once biggest puffin colonies in the world, in the south and south-west of Iceland, are in dire straits. Puffins can live to 35 years and one or two years without breeding may not affect their long-term outlook. However, in Iceland and the Faroes, where their local supply of sandeels has vanished, they have had almost no breeding success over the past ten years (Katz, C., 2014; Miles et al., 2015).

Ocean acidification damages plankton

Carbon dioxide is produced by human activities (and by natural sources) such as the combustion of fossil fuels and deforestation. The atmospheric concentration of CO2 has increased by nearly 30 per cent since the age of industrialization (Vitousek et al., 1997). About ten gigatonnes of carbon dioxide enters the atmosphere each year. The effects would be far worse if it were not for the ability of oceans to absorb more than a quarter the CO2 (26 per cent) of all the carbon dioxide put into the atmosphere (Le Quéré et al., 2015). Unfortunately, this process causes oceans to become acidified because when CO2 dissolves in seawater the pH decreases with a by-product of carbonic acid. The natural buffering chemistry that maintains the balance of the ocean as that of slightly alkaline is now being overwhelmed (Brierley, A. S., and Kingsford, M. J., 2009).

The first direct evidence that ocean acidification was the cause of Earth’s worst mass extinction was found by geologists examining carbonate-bearing limestone in the United Arab Emirates. They discovered the signature of acidification on the boundary between the Permian and Triassic periods of 250m years ago when 90 per cent of species became extinct (Clarkson, et al., 2015).

About 150 years ago the pre-industrial alkaline-acid balance of the oceans was about 8.25. Since then there has been a 0.1 decrease in the pH and they are now about 25 per cent more acidic. A decrease of 0.1 might not sound very much but it is in fact a huge amount because the figure is logarithmic. The rate of acidification is greater than originally thought (Penman et al., 2014).

Acidity of the ocean surface has increased by almost 30 per cent with most of the increase occurring over the past 50 years. If current trends continue, by 2100 it will have increased by as much as 150 per cent (UK Ocean Acidification Research Programme Knowledge Exchange Office, 2016).

Ocean acidification together with changes in prey availability might already be affecting the seabird fauna in Scotland and elsewhere (Orr, et al., 2005; Hays, et al., 2005). Ocean acidification affects phytoplankton and zooplankton whose shells are created from calcium. Acid interferes with the creation of new shells and dissolves those that are created. In the Southern Ocean krill depend on phytoplankton. Krill are declining, with a knock-on effect on other species such as whales and penguins. The fauna in both the Arctic and Antarctic Oceans are likely be affected by increased acidity (Fabry, et al., 2008; Dutkiewicz, et al., 2015; WWF, 2015).

Global warming and ocean acidification appears to be happening ‘slowly’ on a human time-scale, but the actual rate is fast. On an Earth system time-scale it is happening at a rate that is either equal to or exceeds anything ever seen in the past, even with mass extinctions.

Additional threats for seabirds in the North Sea and worldwide

The discard ban is having an impact

The European Union fish discard ban came into force in January 2015. When fishing fleets discard fish and offal it results in large increases in the numbers of scavenging seabirds. Reductions is discards may be resulting in increased predation on some of the smaller seabirds by those that would otherwise scavenge on discards which could result in changes in community structure. In Shetland in the ten years prior to 2003 there was a 50 per cent drop in kittiwake numbers. This was partly attributed to increased predation by the great skua (Stercorarius skua) that normally feeds on sandeels and discards. Kittiwakes are affected directly by reduced breeding success and indirectly by increased predation when sandeel stocks are low (Furness, 2003; Furness, 2010).

Industrial fishing

Industrial fishing has an impact on seabird populations by altering the food-web, changing seabird community composition, reducing stock biomass, and affecting recruitment into the fished stock. Problems can occur when overfishing reduces the fish stock biomass so that it cannot support seabird breeding success. Additionally, it can alter the food-web structure by removing a key species or a preyed-on fish while leaving an unfished one to become more abundant. In the late 1950s sandeels become a target for industrial fishing in the North Sea. This peaked in 1998 when 67 per cent were removed from the population (18,000,000 tons). The declining abundance of sandeels was linked to reductions in numbers of the commercial fish that feed upon them and seabird breeding failures. In 2000 this led to experts resorting to a precautionary closure of fisheries on the north-east coast of the UK (Furness, 2003) which was found to benefit kittiwakes (Daunt et al., 2008). Increasing the numbers of fisheries or fishing for larger quantities of sandeels could have complex ecological consequences for seabirds (Engelhard, et al., 2014).

Long-line bycatch is considered to be the most serious global seabird-fishery issue. It kills annually approximately 100,000 albatrosses. When long lines are deployed behind fishing boats, birds accidently swallow hooks and drown. Many of the species caught are endangered and could become extinct if trends continue (Furness, 2003; Furness, 2010).

Pursuit-diving seabird populations can suffer high mortality rates caused by sea-net bycatch. The birds get tangled in unseen monofilament nets. Declines are worse where gillnets are used near major breeding colonies (Furness, 2003; Furness, 2010).

Plastic pollution

The threat of plastic pollution to seabirds is global and increasing. They are vulnerable to harm from both ingestion and entanglement. Plastic circulating in a marine environment is not exposed to sufficient levels of ultra-violet light and bacterial activity to degrade and may persist for centuries. Production of plastic is increasing exponentially and has doubled every 11 years since commercial production began in the 1950s. Concentrations in oceans have reached 580,000 pieces per kilometre, a large proportion of which is removed by marine organisms acting as a major sink.

Studies carried out from 1962 to 2012 proved that 80 out of 135 (59 per cent) of seabird species had ingested plastic. If governments implement effective waste management the threat will be reduced. A simple model can be used within monitoring programmes to evaluate the effects of management changes. However, if the situation does not improve, then by 2050 some 99 per cent of species will have eaten plastic which will result in changes in mortality or reproduction (Wilcox et al., 2015).

How to halt seabird declines

The outlook is bleak. In the UK declines may have been caused by two factors; industrial fishing of sandeels and climate change. Worldwide, other factors that have a major impact on seabird populations include: fishing for the prey that seabirds eat; catching seabirds with fishing gear; and polluting their environments and introducing predators to breeding colonies (Croxall, et al., 2012). Some species are affected by multiple issues. For example, all of the 22 species of albatross are red-listed by the IUCN. Albatross losses are caused by rats and feral cats eating eggs, chicks and nesting adults, pollution, a serious decline in fish stocks attributed to overfishing and longline fishing (Anderson et al., 2011; IUCN, 2016).

Michelle Paleczny of the University of British Columbia was asked in an interview what could be done to halt seabird decline. She responded that her study underlined the fact that seabird decline is a global issue because they are a wide-ranging group of animals that cross many different boundaries. Their ranges include many different countries within their lifetimes or within their annual cycles. Larger scale marine protective areas are therefore needed with countries cooperating to create a larger network of marine protective areas. The big threats (entanglement of seabirds in fishing gear; human competition with seabirds for small energy-rich fish; and the introduction of predators such as rats and cats and other major impacts on populations) can be resolved by large scale collaboration.

 Another major improvement would be to work on a larger scale to reduce oil and carbon dioxide pollution which in turn affects climate change, which has a negative effect on seabirds.

The important thing is to get firm commitment from governments and to work internationally to reduce threats and to monitor seabirds.

Michelle Paleczny’s comments are reflected by others. Researchers have created models to forecast the number of species that will become extinct in what has been forecast as the sixth mass extinction in Earth’s history. To obtain an accurate global forecast will require coordinated, long-term collaboration by different research groups working on large meta-studies encompassing the many components of variability (biodiversity, time and space scale, and models) (Bellard et al., 2012).

 Richard Price is a freelance journalist specialising in environmental issues.

Acknowledgements

The author would like to thank the following academics for interviews and/or background information by way of academic papers and emails:

  • Nicholas Owens, Director of the Sir Alister Hardy Foundation for Ocean Science (SAPHOS)
  • Dr Richard Burkmar, Tomorrow's Biodiversity Project Officer, Field Studies Centre.
  • Dr Euan Dunn, chief marine adviser at the Royal Society for the Protection of Birds.
  • Dr Debbie Russell, a research fellow with the Scottish Oceans Institute at St Andrews University
  • Michelle Paleczny, MSc., University of British Columbia
  • Rachel Wood, Carbonate Geoscientist, Edinburgh University
  • Simon Foster, Policy & Advice Officer, Scottish Natural Heritage
  • Furness, Institute of Biomedical and Life Sciences, University of Glasgow

References

Anderson, O. R., Small, C. J., Croxall, J. P., Dunn, E. K., Sullivan, B. J., Yates, O. and Black, A., 2011. Global seabird bycatch in longline fisheries. Endangered Species Research, 14(91), pp.91-106.

Arnott, S. A. and Ruxton, G. D., 2002. Sandeel recruitment in the North Sea: demographic, climatic and trophic effects. Marine Ecology Progress Series, 238, pp.199-210.

Beaugrand, G., Brander, K. M., Lindley, J. A., Souissi, S., Reid, P. C. (2003) Plankton effect on cod recruitment in the North Sea. Nature 426: 661–664.

Beaugrand, G., Edwards, M., Brander, K., Luczak, C. and Ibanez, F., 2008. Causes and projections of abrupt climate‐driven ecosystem shifts in the North Atlantic. Ecology letters, 11(11), pp.1157-1168.

Beaugrand, G., Conversi, A., Chiba, S., Edwards, M., Fonda-Umani, S., Greene, C., Mantua, N., Otto, S. A., Reid, P.C., Stachura, M. M. and Stemmann, L., 2015. Synchronous marine pelagic regime shifts in the Northern Hemisphere. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 370(1659), p.20130272.

Barange, M., Beaugrand, G., Harris, R., Perry, R. I., Scheffer, M. and Werner, F., 2008. Regime shifts in marine ecosystems: detection, prediction and management. Trends in Ecology & Evolution, 23(7), pp.402-409.

Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. and Courchamp, F., 2012. Impacts of climate change on the future of biodiversity. Ecology letters, 15(4), pp.365-377.

Brierley, A. S. and Kingsford, M. J., 2009. Impacts of climate change on marine organisms and ecosystems. Current Biology, 19(14), pp. R602-R614.

Clarkson, M. O., Kasemann, S. A., Wood, R. A., Lenton, T. M., Daines, S., Richoz, J. S., Ohnemueller, F., Meixner, A., Poulton, S. W., and Tipper E. T.  Ocean acidification and the Permo-Triassic mass extinction. Science 10 April 2015: 229-232.

Clode, D. and Macdonald, D. W., 2002. Invasive predators and the conservation of island birds: the case of American mink Mustela vison and terns Sterna spp. in the Western Isles, Scotland. Bird Study, 49(2), pp.118-123.

Croxall, J. P., Butchart, S. H. M., Lascelles, B., Stattersfield, A.  J., Sullivan, B., Symes, A, and Taylor, P. (2012). Seabird conservation status, threats and priority actions: a global assessment. Bird Conservation International, 22, pp 1-34. doi:10.1017/S0959270912000020.

Daunt, F., Wanless, S., Greenstreet, S. P., Jensen, H., Hamer, K. C. and Harris, M. P., 2008. The impact of the sandeel fishery closure on seabird food consumption, distribution, and productivity in the north-western North Sea. Canadian journal of fisheries and aquatic sciences, 65(3), pp.362-381.

Dutkiewicz, S., Morris, J. J., Follows, M. J., Scott, J., Levitan, O., Dyhrman, S. T. and Berman-Frank, I., 2015. Impact of ocean acidification on the structure of future phytoplankton communities. Nature Climate Change, 5(11), pp.1002-1006.

Eaton, M., Aebischer, N., Brown, A., Hearn, R., Lock, L., Musgrove, A., Noble, D., Stroud, D. and Gregory, R. (2015) Birds of Conservation Concern 4: The population status of birds in the UK, Channel Islands and Isle of Man. Available at: https://www.britishbirds.co.uk/wp-content/uploads/2014/07/BoCC4.pdf (Accessed: 9 June 2016).

Edwards, M., Helaouet, P., Halliday. N., Beaugrand, G., Fox, C., Johns, D. G., Licandro, P., Lynam, C., Pitois, S., Stevens, D., Coombs, S & Fonseca, L. 2011. Fish Larvae Atlas of the NE Atlantic. Results from the Continuous Plankton Recorder survey 1948-2005. Sir Alister Hardy Foundation for Ocean Science. 22p. Plymouth, U.K. ISBN No: 978-0-9566301-2-7

Engelhard, G. H., Peck, M. A., Rindorf, A., Smout, S. C., van Deurs, M., Raab, K., Andersen, K. H., Garthe, S., Lauerburg, R. A., Scott, F. and Brunel, T., 2014. Forage fish, their fisheries, and their predators: who drives whom?. ICES Journal of Marine Science: Journal du Conseil, 71(1), pp.90-104.

Fabry, V. J., Seibel, B. A., Feely, R. A. and Orr, J. C., 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science: Journal du Conseil, 65(3), pp.414-432.

Furness, R. W. & Tasker, M. L. (2000) Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance and identification of key areas of or sensitive seabirds in the North Sea. Marine Ecology Progress Series, 202, 253-264.

Furness, R. W. (2003). Impacts of fisheries on seabird communities. Scientia Marina, 67 (Suppl. 2), 33-45.

Furness, R. W. (2010). Scottish seabird predator-prey relationships. In Species Management: Changes and Solutions for the 21st Century, ed. by J. M. Baxter and C. A. Galbrith. TSO Scotland, Edinburgh. Pp. 379-394.

Frederiksen, M., Wright, J., Heubeck, M., Harris, M. P., Mavor, R. A. & Wanless, S. (2005) Regional patterns of kittiwake Rissa tridactyla breeding success are related to variability in sandeel recruitment, Marine Ecology Progress Series, 300, 201-211.

Frederiksen, M., Edwards, M., Richardson, A. J., Halliday, N. C. and Wanless, S. (2006), From plankton to top predators: bottom-up control of a marine food web across four trophic levels. Journal of Animal Ecology, 75: 1259–1268.

Frederiksen, M., Edwards, M., Mavor, R. A. and Wanless, S., 2007. Regional and annual variation in black-legged kittiwake breeding productivity is related to sea surface temperature. MARINE ECOLOGY-PROGRESS SERIES-, 350, p.137.

Frederiksen, M., Daunt, F., Harris, M. P. and Wanless, S., 2008. The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long‐lived seabird. Journal of Animal Ecology, 77(5), pp.1020-1029.

Gaston, A. J. and Elliott, K. H., 2013. Effects of climate-induced changes in parasitism, predation and predator-predator interactions on reproduction and survival of an Arctic marine bird. Arctic, pp.43-51.

Goberville, E., Beaugrand, G. and Edwards, M., 2014. Synchronous response of marine plankton ecosystems to climate in the north-east Atlantic and the North Sea. Journal of Marine Systems, 129, pp.189-202.

JNCC (2015) Seabird Population Trends and Causes of Change: 1986-2014 Report (http://www.jncc.defra.gov.uk/page-3201). Joint Nature Conservation Committee. Updated October 2015. Accessed [13 December 2015].

Katz, Cheryl. 2014. Iceland's Seabird Colonies Are Vanishing, With "Massive" Chick Deaths. [ONLINE] Available at: http://news.nationalgeographic.com/news/2014/08/140827-seabird-puffin-tern-iceland-ocean-climate-change-science-winged-warning/. [Accessed 9 June 2016].

Hays, G. C., Richardson, A. J. and Robinson, C., 2005. Climate change and marine plankton. Trends in Ecology & Evolution, 20(6), pp.337-344.

Heath, M., Edwards, M., Furness, R., Pinnegar, J., and  Wanless, S.  (2009). A view from above: changing seas, seabirds and food sources in Marine Climate Change Ecosystem Linkages Report Card  2009.  (Eds.  Baxter, J. M., Buckley, P. J and Frost, M. T.) Online science reviews, 24pp. www.mccip.org.uk/elr/view        

Heath, M. R., Neat, F. C., Pinnegar, J. K., Reid, D. G., Sims, D. W. and Wright, P. J., 2012. Review of climate change impacts on marine fish and shellfish around the UK and Ireland. Aquatic Conservation: Marine and Freshwater Ecosystems, 22(3), pp.337-367.

Hinder, S. L., Gravenor, M. B., Edwards, M., Ostle, C., Bodger, O. G., Lee, P. L., Walne, A. W. and Hays, G. C., 2014. Multi‐decadal range changes vs. thermal adaptation for north-east Atlantic oceanic copepods in the face of climate change. Global change biology, 20(1), pp.140-146.

Irons, D. B., Anker-Nilssen, T., Gaston, A. J., Byrd, G. V., Falk, K., Gilchrist, G., Hario, M., Hjernquist, M., Krasnov, Y. V., Mosbech, A., Olsen, B., Petersen, A., Reid, J. B., Robertson, G. J., Strøm, H. and Wohl, K. D. (2008), Fluctuations in circumpolar seabird populations linked to climate oscillations. Global Change Biology, 14: 1455–1463.

Lancaster, J. (Ed.), McCallum, S., Lowe A. C., Taylor, E., Chapman A. & Pomfret, J. (2014). Development of detailed ecological guidance to support the application of the Scottish MPA selection guidelines in Scotland’s seas. Scottish Natural Heritage Commissioned Report No.491. Sandeels – supplementary document.

Lanchbery, J., 2006. Climate change-induced ecosystem loss and its implications for greenhouse gas concentration stabilisation. Avoiding Dangerous Climate Change, p.143.

Le Quéré, C., Moriarty, R., Andrew, R. M., Peters, G. P., Ciais, P., Friedlingstein, P., Jones, S. D., Sitch, S., Tans, P., Arneth, A. and Boden, T. A., 2015. Global carbon budget 2014.

IUCN. 2016. The IUCN Red List of Threatened Species. Version 2015-4. [ONLINE] Available at: HTTP://www.iucnredlist.org. [Accessed 9 June 2016]

MacDonald, A., Heath, M. R., Edwards, M., Furness, R. W., Pinnegar, J. K., Wanless, S., Spiers, D. C. and Greenstreet, S. P., 2015. Climate-driven trophic cascades affecting seabirds around the British Isles. Oceanography and Marine Biology: An Annual Review, 53, pp.55-79.

MSA, 2021, Marine Scotland Assessment [ONLINE] Available at: https://marine.gov.scot/sma/assessment/seabirds-0. [Accessed 24 August 2021].

Miles, W. T., Mavor, R., Riddiford, N. J., Harvey, P. V., Riddington, R., Shaw, D. N., Parnaby, D. and Reid, J. M., 2015. Decline in an Atlantic Puffin Population: Evaluation of Magnitude and Mechanisms. PloS one, 10(7), p.e0131527.

Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F. and Key, R. M., 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437(7059), pp.681-686.

Oswald, S. A., Huntley, B., Collingham, Y. C., Russell, D. J. F., Anderson, B. J., Arnold, J. M., Furness, R. W. and Hamer, K. C. (2011), Physiological effects of climate on distributions of endothermic species. Journal of Biogeography, 38: 430–438.

Paleczny, M., Hammill, E., Karpouzi, V., Pauly, D. (2015) Population Trend of the World’s Monitored Seabirds, 1950-2010. PLoS ONE 10(6): e0129342.doi:10.1371/journal.pone.0129342

Parsons, M., Mitchell, I., Butler, A., Ratcliffe, N., Frederiksen, M., Foster, S. and Reid, J. B., 2008. Seabirds as indicators of the marine environment. ICES Journal of Marine Science: Journal du Conseil, 65(8), pp.1520-1526.

Parsons, M., Mitchell, I., Butler, A., Ratcliffe, N., Frederiksen, M., Foster, S. and Reid, J. B., 2008. Seabirds as indicators of the marine environment. ICES Journal of Marine Science: Journal du Conseil, 65(8), pp.1520-1526.

Penman, D. E., Hönisch, B., Zeebe, R. E., Thomas, E. and Zachos, J. C., 2014. Rapid and sustained surface ocean acidification during the Paleocene‐Eocene Thermal Maximum. Paleoceanography, 29(5), pp.357-369.

Planque, B., and Batten, S. D., 2000. Calanus finmarchicus in the North Atlantic: the year of Calanus in the context of interdecadal change. ICES Journal of Marine Science: Journal du Conseil, 57(6), pp.1528-1535.

Solomon, S., Plattner, G. K., Knutti, R. and Friedlingstein, P., 2009. Irreversible climate change due to carbon dioxide emissions. Proceedings of the national academy of sciences, pp.pnas-0812721106.

SNH. 2012. Scottish Natural Heritage Trend Note for Seabirds in Scotland No. 21, October 2012 [ONLINE] Available at: http://www.snh.gov.uk/docs/B1163280.pdf. [Accessed 30 June 2016]

SNH. 2014. Scottish Natural Heritage Science Newsletter, Issue 11 - December 2014. [ONLINE] Available at: http://www.snh.gov.uk/docs/A1477963.pdf. [Accessed 9 June 2016].

SNH (2016a) Scottish National Heritage Biodiversity Indicator S005, March 2016

http://www.snh.gov.uk/docs/B424907.pdf

SNH (2016b). Scottish Natural Heritage Science Newsletter, Issue 15 - March 2016. [ONLINE] Available at: http://www.snh.gov.uk/docs/A1917258.pdf. [Accessed 9 June 2016].

Russell, D. J. F., Wanless, S., Collingham, Y. C., Anderson, B. J., Beale, C., Reid, J. B., Huntley, B. and Hamer, K. C. (2015), Beyond climate envelopes: bio-climate modelling accords with observed 25-year changes in seabird populations of the British Isles. Diversity Distributions., 21: 211–222.

Reid, P. C., Hari, R. E., Beaugrand, G., Livingstone, D. M., Marty, C., Straile, D., Barichivich, J., Goberville, E., Adrian, R., Aono, Y. and Brown, R., 2015. Global impacts of the 1980s regime shift. Global change biology.

Thompson, P. M., Ollason, J. C. (2001) Lagged effects of ocean climate change on fulmar population dynamics. Nature 413: 417–420. doi: 10.1038/35096558

UK Ocean Acidification Research Programme Knowledge Exchange Office. 2016. UK Ocean Acidification Research Programme. [ONLINE] Available at: http://www.oceanacidification.org.uk/Home. [Accessed 5 June 2016].

Vitousek, P. M., Mooney, H. A., Lubchenco, J. and Melillo, J. M., 1997. Human domination of Earth's ecosystems. Science, 277(5325), pp.494-499.

Wanless, S., Harris, M. P., Redman, P. & Speakman, J. (2005) Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Marine Ecology Progress Series, 294, 1-8.

Wilcox, C., Van Sebille, E. and Hardesty, B. D., 2015. Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proceedings of the National Academy of Sciences, 112(38), pp.11899-11904.

Wright, P. J. and Bailey, M. C., 1996. Timing of hatching in Ammodytes marinus from Shetland waters and its significance to early growth and survivorship. Marine Biology, 126(1), pp.143-152.

Wright, P. J., Jensen, H. and Tuck, I., 2000. The influence of sediment type on the distribution of the lesser sandeel, Ammodytes marinus. Journal of Sea Research, 44(3), pp.243-256.

WWF. 2015. Living Blue Planet Report. Species, habitats and human well-being. [Tanzer, J., Phua, C., Lawrence, A., Gonzales, A., Roxburgh, T. and P. Gamblin (Eds)]. WWF, Gland, Switzerland.

[1] From this point on the word ‘sandeel’ is used instead of ‘the lesser sandeel’ (Ammodytes marinus).

[2] From this point on the black-legged kittiwake is the kittiwake.

Close

50% Complete

Two Step

Lorem ipsum dolor sit amet, consectetur adipiscing elit, sed do eiusmod tempor incididunt ut labore et dolore magna aliqua.