Marine conservation in a rapidly changing world

Authors


Steve Hawkins, Ocean and Earth Science, University of Southampton, Waterfront Campus, European Way, Southampton, SO14 3ZH, UK. E–mail: S.J.Hawkins@soton.ac.uk

GLOBAL ENVIRONMENTAL CHANGE

The Earth and its oceans are going through a period of unprecedented change driven by increasing human population and economic development. Increasing greenhouse gases are influencing climate; temperatures are rising (IPCC, 2007; Burrows et al., 2011); sea levels are rising and conditions are getting stormier (Lowe and Gregory, 2005); stratification of shelf seas may intensify (Richardson and Schoeman, 2004); ocean circulation patterns may change (Bryden et al., 2005). While not strictly a climate effect, increased carbon dioxide in the atmosphere is leading to a reduction of the pH of the oceans (‘Ocean Acidification’) (Caldeira and Wickett, 2003; Orr et al., 2005).

Superimposed on these physical and chemical changes are biological impacts at global scales such as homogenization of floras and faunas by species invading from other biogeographic realms (Maggs et al., 2010) and overfishing of large pelagic species (Myers and Worm, 2005). Marine plastic litter is a global problem (Thompson et al., 2004). On a regional scale all seas are showing signs of overfishing for demersal species and to some extent smaller pelagic species. Some enclosed seas (e.g. Baltic, N. Adriatic) are showing the impacts of eutrophication which can interact with fishing to reshape ecosystems (Österblom et al., 2007). Local scale impacts are myriad from point source pollution, recreational use of coastal areas, marine noise and most pervasive of all, coastal development leading to habitat degradation and total loss (Airoldi and Beck, 2007). Such local degradation can scale up to whole regions (i.e. coastal defences in the Northern Adriatic and the southern North-Sea, Airoldi et al., 2005).

In this brief article I will consider the major issues facing marine conservation in a rapidly changing world. I will outline an approach based on managing the interactions between global climate change and other global, regional and local impacts. This builds on work published elsewhere (Hiscock et al., 2004; Hawkins et al., 2008, 2009, 2010a,2010b; Firth and Hawkins, 2011). I will then give some brief pointers for the way forward for conservation including marine protected areas (MPAs). The crucial need for understanding connectivity better is emphasized. As this article has a 10–25 year time horizon, I will not consider the longer-term threat of reducing pH of the ocean as much has been written about ‘Ocean Acidification’ elsewhere, although some recent work has suggested that effects may already be occurring (Wootton et al., 2008).

IMPLICATIONS OF CLIMATE CHANGE FOR MARINE CONSERVATION

There is much evidence for responses of marine biodiversity and ecosystems to past climate fluctuations and present day rapid climate change (Parmesan, 2006). Species are moving polewards: with advance and increase in abundance of warm water species and retreat and reduction in abundance of cold water species (Beaugrand et al., 2002; Genner et al., 2004, 2010; Perry et al., 2005; Helmuth et al., 2006). Fish are moving into deeper water (Dulvy et al., 2008). Some high latitude species may have nowhere to go. This is also the case in enclosed seas such as the Mediterranean, where recent mass mortality events have occurred (Coma et al., 2009) especially the Adriatic (Conversi et al., 2009). Assemblage composition and community structure is changing with consequences for ecosystem functioning (for intertidal examples see Hawkins et al., 2009).

For example on rocky shores in north-west Europe, fast growing northern species of barnacle (Semibalanus balanoides) and limpet (Patella vulgata) are being replaced with slower growing southern species (Chthamalus spp., P. depressa, Moore et al., 2007; Poloczanska et al., 2008; Wethey et al., 2011). Canopy cover of fucoid algae will decrease in the north and shores will resemble those of southern Europe with scarce macroalgae on the mid-shore (Ballantine, 1961; Hawkins and Hartnoll, 1983a; Coleman et al., 2006). This will be due to a variety of factors including increased temperature and wave action (Hawkins et al., 2009). Greater stress on early life history stages will make escapes from grazers less likely (Coleman et al., 2006); this will be compounded by greater grazing intensity by more species of grazers and with an extended window of seasonal activity (Jenkins et al., 2001; Hawkins et al., 2008, 2009). These shifts will reduce the productivity of the shore with less macroalgal biomass for export as detritus (Hawkins et al., 2008, 2009). Ecosystem engineers such as canopy algae are also important facilitators of less stressful conditions when the tide is out (Moore et al., 2007) as well as habitat providers (Thompson et al., 1996).

Conservation management must take into account a shifting baseline. This will influence both species and site designations and management plans. Some species enjoying protected status in the UK are actually range edge species (e.g. the giant goby, Gobius cobitis – which is a southern species) that will do much better in a warming world. Perhaps its conservation status needs to be re-examined. In Special Areas of Conservation (SACs) designated under the EU Habitats Directive species composition will change. Without long-term and broad-scale contextual monitoring it will be difficult to assess whether such changes are a result of climate change or local impacts. In many cases changes will be positive (e.g. recent increases in the reef-building worm Sabellaria alveolata around much of the coast of England and Wales (Frost et al., 2006)). Northern species such as the horse mussel, Modiolus modiolus and the sea-fan Swiftia pallida will be at risk (Hiscock et al., 2004 for further details) with consequences for other species, especially in the case of Modiolus which is an ‘ecosystem-engineer’ providing habitat for a variety of other species.

Establishment of marine protected areas (MPAs) in appropriate networks will help species to retreat (or expand if conditions get colder). It is also important that the areas between such reserves do not become so degraded that they become barriers to passage between reserves; species have different dispersal capabilities and thus relying on reserves alone as sources and sinks of propagules will not be enough (Gaines et al., 2003; Johnson et al., 2008). Unlike terrestrial systems where pockets of species can have nowhere to go due to habitat fragmentation and loss, the more open nature of the marine ecosystems means that planktonic (Beaugrand et al., 2002) and fish species (Genner et al., 2004, 2010; Perry et al., 2005; Simpson et al., 2011) are able to migrate northwards. In contrast, most benthic species including those from estuaries and the shore, patches of favourable habitat are linked by larval dispersal. The exceptions are those with direct development (e.g. whelks such as Buccinum undatum and Nucella lapillus). Rafting can be an important dispersal mechanism for species with direct development (Johnson et al., 2001). Migration of benthic species (especially intertidal and estuarine) can be difficult as they often have to cross unfavourable patches of habitat; therefore they are more like terrestrial or freshwater species where dispersal is limited and habitats are often fragmented. Expansion of species can be inhibited by hydrographic barriers and gaps between suitable habitat (Gaylord and Gaines, 2000; Keith et al., 2011). Understanding of larval dispersal and connectivity of favourable habitat patches and meta-populations is crucial in understanding responses to climate change.

STRATEGIC MANAGEMENT

Non-natives

Little can be done about climate change over the next 50 years due to the inertia in the climate system – even if there was a rapid shift away from a carbon-based economy (Solomon et al., 2009). What can, however, be managed is the interaction between global climate change and other impacts such as non-native species.

One of the most pressing issues is the interactions between invasive species from other biogeographic realms (global homogenization) and climate change (Thompson et al., 2002; Branch et al., 2008); there is good evidence that climate change favours non-native species (Stachowicz et al., 2002; Sax et al., 2007). This can only be tackled by greater bio-security and vigilance against both deliberate and accidental introductions. A cautionary tale is the Pacific oyster, Crassostrea gigas; this was introduced to many other places globally in the 1960s and 1970s for cultivation. In the UK it was deliberately introduced by the Government (Ministry of Agriculture, Fisheries and Food). At the time in the 1960s it was believed it could only be hatchery reared as it was too cold for it to breed in the wild. Since then conditions have become warmer and it is now spreading widely and forming reef like structures in the Netherlands and at some sites in the UK (e.g. the Yealm estuary). In the Netherlands it has displaced mussel fisheries in some areas (Nehls et al., 2006).

Eutrophication

Nutrient enrichment leading to eutrophication can occur both at regional (i.e. in semi-enclosed seas such as the Irish Sea (Allen et al., 1998); the Northern Adriatic (Crema et al., 1991); and the Baltic (Suikkanen et al., 2007)) as well as on more local scales (i.e. individual bays, lagoons or estuaries). The intensity and frequency of occurrence of algal blooms, including potential harmful species, is more likely in a warming world. A combination of elevated nutrients and highly stable water columns due to warm weather were thought to be responsible for triggering the Chrysolepsis bloom in the Skagerrak in 1988 which led to massive losses to the aquaculture industry as well as causing widespread mortality of benthic species and fish (Richardson and Heilmann, 1995). There is some evidence of increased frequency of harmful algal blooms worldwide (Hallegraeff, 1993; Van Dolah, 2000; Jöhnk et al., 2007) which may reflect the interaction of coastal eutrophication and climate change increasing the likelihood of their occurrence (Hallegraeff, 2010). In more enclosed lagoons and estuaries, warmer weather, greater flows of fresh water in winter and elevated nutrients may all lead to more rapid proliferation of ephemeral algal blooms (Jöhnk et al., 2007); although hotter and dryer summers may have the reverse effect especially for the intertidal species which can become bleached high on the shore (Hawkins and Hartnoll, 1983b).

While climate change cannot be dealt with, excessive nutrient input can be managed. Eutrophication is being controlled in Europe via a series of European Directives (Urban Water Directive, Water Framework Directive, etc.). This is one example where active management is likely to reduce the effects of climate change by concentrating on that part of the interaction that can be effectively dealt with.

Overfishing

It has long been known that climate fluctuations have driven changes in fish stocks worldwide (classic work by Cushing, 1975; Cushing and Dickson, 1976; see Mieszkowska et al., 2009 for a recent review of cod) and in European and British waters (Russell et al., 1971; Southward, 1980; Southward et al., 1988, 1995, 2005; Hawkins et al., 2003). This is primarily mediated through recruitment processes (Koslow et al., 1987; Beaugrand et al., 2003; Olsen et al., 2011). Pelagic species are particularly driven by climate fluctuations with classic fluctuations occurring between herrings and pilchards being recorded from the English Channel (the so-called Russell Cycle – Cushing and Dickson, 1976). Recent work has shown that demersal species can also be driven by climate (Genner et al., 2004; Perry et al., 2005; Simpson et al., 2011), but fishing also plays a key role especially for larger bodied species (Genner et al., 2010). Reduction in fished spawning stock biomass can make them more susceptible to mismatch with larval food post spawning (Cushing, 1975). Climate change can also increase chances of mismatch by altering both type (i.e. the wrong species of copepod, Beaugrand et al., 2003) and timing of food (Edwards and Richardson, 2004). Thus climate change, coupled with reduced spawning biomass is likely to interact to increase the frequency of poor recruitment years (Sumaila et al., 2011). Therefore for a northern species a more precautionary approach should be taken, while expanding stocks of southern species could provide stocks less sensitive to fishing pressure.

Habitat alteration, loss, and degradation

Rising sea level and stormier seas will alter the configuration of coastlines with inevitable change in the distribution and quality of habitats as erosional processes increase (Slott et al., 2006). Society will respond by protecting coastal infrastructure such as roads and railways as well as homes by building sea defences (Airoldi et al., 2005). This will lead to a hardening of the coast and a proliferation of coastal defence structures of various kinds (Moschella et al., 2005; Bulleri and Chapman, 2010; Chapman and Underwood, 2011) which will have impacts on adjacent soft sedimental communities and fish nursery grounds (Martin et al., 2005). Such structures also provide new rocky shore habitat for both native and non-native species (Martins et al., 2010; Airoldi and Bulleri, 2011). There is some evidence that such structures have acted as stepping stones for species advancing along the south coast of England (Helmuth et al., 2006; Mieszkowska et al., 2006; Hawkins et al., 2009) where lack of suitable rocky habitat was thought to have been one of the factors setting boundaries for several species between Portland and the Isle of Wight (Crisp and Southward, 1958; Keith et al., 2011). They have also been shown to aid proliferation of invasive non-native species (Airoldi and Bulleri, 2011). Minor enhancements to such structures can increase their value as a habitat for enhancement of biodiversity by incorporating rock pools (Chapman and Blockley, 2009), or by enhancing topographic complexity (Martins et al., 2010).

Overall such structures are less diverse than natural rocky shores, probably due to a combination of lack of extent and much lower habitat complexity combined with scouring as they often interface with high energy, sandy or gravelly shores (Moschella et al., 2005; Bulleri and Chapman, 2010). While little can be done about rising sea levels over the next 25–50 years, care should be exercised in adapting to such changes. Environmentally sensitive design of hard structures can minimize impacts on surrounding habitat and can maximize opportunities for colonization of desired hard substratum species and assemblages (Burcharth et al., 2007).

Non-engineered options are also available, such as managing retreat or using natural sea defences (Hulme, 2005). Potentially good examples are saltmarshes, which can be managed to maximize their role in combating coastal erosion. Many marshes in the UK and Europe are grazed. By managing pastoral grazing regimes the ecosystem services provided by saltmarshes could be optimized to maximize their potential for wave attenuation and sediment trapping. The lower the grazing pressure the greater the vegetation height and biomass. Thus the adaptational framework can be addressed by simple measures. A contribution to mitigation of climate change may also be possible too. Saltmarshes sequester carbon as peat and there again is potential to manage marshes in such a way as to maximize carbon storage (Gedan et al., 2011).

LOOKING FORWARD

Over the next 50 years or so climate will continue to change. A major policy challenge will be if there is a short cold period as occurred in the 1960s to the late 1980s in Northern Europe. This may mask longer-term warming and lead to greater climate scepticism among the general population and politicians alike. There is also a possibility of a rapid shift to much colder conditions due to changes in the thermohaline circulation (Bryden et al., 2005) prompted by lower salinity water in polar regions. The Younger-Dryas period (12 800 and 11 500 years before present) was such an extremely cold period which halted and reversed warming following the end of the last Ice Age.

Whatever happens, long-term monitoring is essential to segregate out short-term weather-driven noise from more directional climate change effects (Hawkins et al., 2003; Southward et al., 1995, 2005; Schiel, 2011). Such information is invaluable for adaptive management and is always at risk at times of financial stringency (many long-term monitoring programmes were stopped in the 1980s). In adapting to climate change it is important to focus on managing interactions of climate change with those other impacts that we can manage. Greater biosecurity and a much more precautionary approach to aquaculture introductions would greatly reduce threats from invasive non-native species. Reducing nutrient inputs to enclosed waters can reduce the risk of eutrophication and likelihood of harmful algal blooms. Carefully managing fishing in the context of climate change can prevent stock crashes. Habitat loss and degradation should be avoided by careful planning and ensuring that local concerns do not scale up to whole coastlines (e.g. the Northern Adriatic; Airoldi et al., 2005).

ACKNOWLEDGEMENTS

This publication has benefitted from the direct input of Moira MacLean and Maria Vale in its assembly and in seeking out correct literature – many thanks to M and M. This work is also the culmination of a team effort building on the groundbreaking work of Alan Southward at the Marine Biological Association of the UK. I have drawn extensively on ideas and joint work with the following in approximate chronological order: Alan and Eve Southward, Mike Kendall, Mike Burrows, Roger Herbert, Richard Thompson, Keith Hiscock, Martin Genner, David Sims, Paula Moschella, Nova Mieszkowska, Pip Moore, Becky Leaper, Jackie Hill, Elvira Poloczanska, Stuart Jenkins, Patricia Masterson, Heather Sugden, Martin Skov and Louise Firth and no doubt many more. This work stems from the MarClim project funded by Countryside Council for Wales, the Crown Estate, Defra, English Nature, Environment Agency, Joint Nature Conservation Committee, UK Climate Impacts Programme, Marine Institute, Scottish Natural Heritage, Scottish Government, States of Jersey and the WWF and NERC via the Marine Biological Association Fellowship Programme and Oceans 2025. Thanks are given to John Baxter who funded some pump priming work by SNH at the Marine Biological Association that kick-started MarClim and much else. Thanks John!

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