Climate Change and Marine Benthos: a Review of Existing Research and Future Directions in the North Atlantic Silvana N.R

Advanced Review Climate change and marine benthos: a review of existing research and future directions in the North Atlantic Silvana N.R. Birchenough,1,∗,† Henning Reiss,2,† Steven Degraer,3,† Nova Mieszkowska,4 Ángel Borja,5 Lene Buhl-Mortensen,6 Ulrike Braeckman,7 Johan Craeymeersch,8 IlseDeMesel,8 Francis Kerckhof,3 Ingrid Kröncke,9 Santiago Parra,10 Marijn Rabaut,7 Alexander Schröder,11 Carl Van Colen,7 Gert Van Hoey,12 Magda Vincx7 and Kai Wätjen13 There is growing evidence that climate change could affect marine benthic systems. This review provides information of climate change-related impacts on the marine benthos in the North Atlantic. We cover a number of related research aspects, mainly in connection to two key issues. First, is the relationship between different physical aspects of climate change and the marine benthos. This section covers: (a) the responses to changes in seawater temperature (biogeographic shifts and phenology); (b) altered Hydrodynamics; (c) ocean acidification (OA); and (d) sea-level rise-coastal squeeze. The second major issue addressed is the possible integrated impact of climate change on the benthos. This work is based on relationships between proxies for climate variability, notably the North Atlantic Oscillation (NAO) index, and the long-term marine benthos. The final section of our review provides a series of conclusions and future directions to support climate change research on marine benthic systems. © 2015 John Wiley & Sons, Ltd. Howtocitethisarticle: WIREs Clim Change 2015. doi: 10.1002/wcc.330 INTRODUCTION ∗Correspondence to: [email protected] he North Atlantic plays a major role in climate 1Lowestoft Laboratory, The Centre for Environment, Fisheries and Tchange as it is a key node in the thermohaline Aquaculture Science , Suffolk, UK circulation. The inflow of cold deep water into the 2 Faculty of Biosciences and Aquaculture, University of Nordland, northern North Atlantic and the consequent transport Bodø, Norway 3Royal Belgian Institute of Natural Sciences, Operational Direc- torate Natural Environment, Marine Ecology and Management, 10Centro Oceanográfico de A Coruña, Instituto Español de Brussels, Belgium Oceanografía, A Coruña, Spain 4Marine Biological Association of the United Kingdom, Plymouth, 11Lower Saxony Water Management Agency, NLWKN, Oldenburg, UK Germany 5Marine Research Division, Azti, Pasaia, Spain 12Research Institute for Agriculture and Fishery research, Depart- 6Institute of Marine Research, PB 1870 Nordnes, N-5817 Bergen, ment of Aquatic Environment and Quality, Bio-Environmental Norway Research Group, Ankerstraat 1, 8400 Oostende, Belgium 7Department of Biology, Research Group Marine Biology, Ghent 13Alfred Wegener Institute for Polar & Marine Research, University, Ghent, Belgium Bremerhaven, Germany 8Institute for Marine Resources and Ecosystem Studies, Wageningen, Netherlands †These authors wish to be considered as joint first authors. 9Department for Marine Research, Senckenberg Institute, Conflict of interest: The authors have declared no conflicts of interest Wilhelmshaven, Germany for this article. © 2015 John Wiley & Sons, Ltd. Advanced Review wires.wiley.com/climatechange of warm surface water to the north ensure that Europe and with wider effects for other ecosystem compo- is much warmer than comparative latitudes elsewhere. nents. This process allows the heat to be transferred to the Our synthesis also summarizes the current state Arctic and contributes to the melting sea ice and to of play with regard to OA, as evidence indicates that the potential release of methane. The North Atlantic the oceans are becoming more acidic. Some studies contains about a quarter of the anthropogenic carbon report that there will be some effects for dedicated stored in the oceans as a result of an inflow of depth groups, whereas there are other studies that do report water and the deep mixing that occurs in this system. limited effects and consequences for benthic systems. Climate change is having an effect in the marine This is an active research area, producing targeted environment. As these changes are being observed, research to understand organisms’ responses to pH it is imperative to understand how marine systems changes in the laboratory and field studies. will be affected under changing climate conditions. We have included a specific emphasis on knowl- Our review concentrates on climate change effects edge gained from former benthic long-term series stud- observed in the benthic communities of the Atlantic ies on the effects of the North Atlantic Oscillation region over the last hundred years.1–9 Marine ben- (NAO) as a proxy for climate variability, as this infor- thic communities are especially suited for long-term mation can be related to similar studies over other comparative investigations as many of the constituent ecosystem components, providing useful insights on species are sessile or have low mobility, are relatively the changes observed in marine benthic communities long lived and so can integrate the effects of environ- over long-term assessments. mental change over time. The macrobenthos has an Finally, the conclusions section provides an important functional role in the reworking of sedi- overview of the current work and also a recommen- ments, provides nutrients and food to higher trophic dation list of gaps where further research is needed. groups and allows the provision of habitats through habitat engineering species, e.g., Refs 10–14. Given the important ecological role of benthic DIRECT AND CIRCUMSTANTIAL communities it is essential to understand and predict EVIDENCE OF CLIMATE how they are likely to respond to climate change. Cli- CHANGE EFFECTS mate change is considered to be a complex problem, as conceptually summarized by the ICES Benthos Ecol- Temperature Change-Driven Effects ogy Working Group (Ref 3; Figure 1). We acknowl- edge that the study of all of these processes is not trivial Distributional Shifts and there will be a need to undertake research with Biogeographic studies have been the focus of much multidisciplinary teams to answer some aspects high- ecological research that has identified a link between lighted in this conceptual framework. Figure 1 is used the distribution of marine species and mean sea surface to describe the main abiotic (e.g., storms and habi- isotherms.15,16 Oceanic changes in temperature due to tat loss) and biotic (e.g., latitudinal shifts of species, global climate change are causing poleward shifts in larval supply, and match/mismatch) effects that will the latitudinal distribution of species toward cooler be affecting benthic and directly interconnected (e.g., marine environmental regions throughout the North plankton) systems. It is clear that there are some wider Atlantic.17 Such distributional shifts have already been aspects (e.g., temperature, OA, and anthropogenic found for several components of the marine ecosys- interactions) will have a wider influence across all of tem: fish,18–21 phytoplankton,22,23 zooplankton,24–26 the components in the framework. Some knowledge and also benthos.27–29 is already available either through directly or circum- There is clear evidence of change in the distri- stantially evidenced effects of climate change onto the bution and abundance of benthic species in response benthos, but there are still aspects that require further to seawater temperature change, e.g., in the North research. The way this review is structured is look- Atlantic.5,7,29–31 Most changes are initially seen to ing at the (expected) ‘knowns’ and consequently also be occurring at the edge of ranges, where organ- the ‘unknowns’, for example looking at existing litera- isms are more likely to be physiologically stressed. ture on how species are changing their distributions in Intertidal organisms, for example, have shown some response of changes in environmental conditions (e.g., of the fastest responses to climate change as they temperature). Furthermore, the effects of sea level rise are living close to their physiological tolerance lim- in intertidal areas (known as ‘the coastal squeeze phe- its. Evidence of a strong climatic influence has been nomenon’) could severely affect benthic habitats with observed in the abundances of the co-occurring inter- direct repercussions for the loss of benthic function tidal Lusitanian barnacles Chthamalus montagui and © 2015 John Wiley & Sons, Ltd. WIREs Climate Change Climate change and marine benthos Abiotic effects Biotic effects Non benthos Benthos First-order effects n-order effects (l) Habitat loss (+) risk of local extinction/ population resilience level Sea- (n) (o) (m) (–) Salinity (intertidal) Increased osmotic stress (o) Pollution River (j) Phytobenthic production run-off (j) Eutrophication ) Cloudiness/ precipitation 2 (i) Irradiance (e,j) (g) (k) (q) Larval supply Changed currents Plankton production Changes in food-web (e,h,j) structure (m) (d,e,h) (t) (+) Stratification (f) Altered benthic and reallocation of fronts pelagic coupling Temperature regime (d) Sediment (i) Wind regime composition Altered community (k) (i) (i) (+) Storminess/ structure/habitat Green house gasses (e.g. CO Turbidity turbulence (i) (c) Match/mismatch (a) Latitudinal shift of species (b) (+) Southern invasive species (+) Secondary production (p) (–) Physiological impact on Acidification calcareous organisms Anthropogenic interactions: (r, s) | 196 FIGURE 1 Conceptual diagram of the effects of climate change and benthic interactions illustrating the influence

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