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Consequences of climate driven biodiversity changes for ecosystem

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Article in Marine Ecology Progress Series · December 2009

DOI: 10.3354/meps08378

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 Vol. 396: 245–259, 2009 MARINE ECOLOGY PROGRESS SERIES
Published December 9
doi: 10.3354/meps08378 Mar Ecol Prog Ser

Contribution to the Theme Section ‘Marine biodiversity: current understanding and future research’
OPEN
ACCESS
Consequences of climate-driven biodiversity
changes for ecosystem functioning of North
European rocky shores
S. J. Hawkins1, 2,*, H. E. Sugden1, N. Mieszkowska2, P. J. Moore2, 3, E. Poloczanska4,
R. Leaper5, R. J. H. Herbert 6, 7, M. J. Genner 2, 8, P. S. Moschella2, 9, R. C. Thompson10,
S. R. Jenkins1, 2, A. J. Southward2,†, M. T. Burrows11
1
School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey LL59 5AB, UK
2
Marine Biological Association of the UK, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
3
School of Natural Sciences, Edith Cowan University, Joondalup, Western Australia 6027, Australia
4
Climate Adaptation Flagship, CSIRO Marine & Atmospheric Research, PO Box 120, Cleveland, Queensland 4163, Australia
5
Commonwealth Environment Research Facilities Program Marine Biodiversity Hub: Prediction Program, Tasmanian
Aquaculture and Fisheries Institute, University of Tasmania, Locked Bag 49, Hobart 7001, Australia
6
Medina Valley Field Centre, Dodnor Lane, Newport, Isle of Wight PO30 5TE, UK
7
School of Conservation Sciences, Bournemouth University, Christchurch House, Talbot Campus, Poole, Dorset BH12 5BB, UK
8
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
9
CIESM – The Mediterranean Science Committee, 16 bd de Suisse, MC 98000, Monaco
10
Marine Biology and Ecology Research Centre, Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK
11
Scottish Association for Marine Sciences, Dunstaffnage Marine Laboratory, Oban, Argyll PA37 1QA, UK

ABSTRACT: We review how intertidal biodiversity is responding to globally driven climate change,
focusing on long-term data from rocky shores in the British Isles. Physical evidence of warming
around the British Isles is presented and, whilst there has been considerable fluctuation, sea surface
temperatures are at the highest levels recorded, surpassing previous warm periods (i.e. late 1950s).
Examples are given of species that have been advancing or retreating polewards over the last 50 to
100 yr. On rocky shores, the extent of poleward movement is idiosyncratic and dependent upon life
history characteristics, dispersal capabilities and habitat requirements. More southern, warm water
species have been recorded advancing than northern, cold water species retreating. Models have
been developed to predict likely assemblage composition based on future environmental scenarios.
We present qualitative and quantitative forecasts to explore the functional consequences of changes
in the identity, abundance and species richness of gastropod grazers and foundation species such as
barnacles and canopy-forming algae. We forecast that the balance of primary producers and sec-
ondary consumers is likely to change along wave exposure gradients matching changes occurring
with latitude, thereby shifting the balance between export and import of primary production.
Increases in grazer and sessile invertebrate diversity are likely to be accompanied by decreasing
primary production by large canopy-forming fucoids. The reasons for such changes are discussed in
the context of emerging theory on the relationship between biodiversity and ecosystem functioning.

KEY WORDS: Climate change · Intertidal · Range shifts · Biodiversity · Ecosystem functioning ·
Northeast Atlantic
Resale or republication not permitted without written consent of the publisher

INTRODUCTION in the distribution of plankton (Beaugrand et al. 2002,

Beaugrand & Reid 2003), fish (Perry et al. 2005, Dulvy
Marine biodiversity and ecosystems are responding et al. 2006), subtidal benthic invertebrates (e.g. Ling et
to global climate change (Southward et al. 1995, Haw- al. 2008, Ling et al. 2009) and intertidal species (see
kins et al. 2003, Parmesan & Yohe 2003). Major shifts Harley et al. 2006, Helmuth et al. 2006 for reviews)

*Email: [email protected] © Inter-Research 2009 · www.int-res.com

†
Deceased
246 Mar Ecol Prog Ser 396: 245–259, 2009

have been recorded in recent years. Coastal and near- assemblage level changes by synthesising summaries
shore biodiversity loss is also occurring due to regional of published work on the role of biological interactions
and local-scale impacts (see e.g. Ling 2008, Polunin in modulating climate change responses (Poloczanska
2008 for reviews) such as overfishing and its side et al. 2008) and give a preliminary report of statistically
effects (Kaiser et al. 2007), pollution (Terlizzi et al. based modelling of the response of functionally impor-
2005), recreational pressures (Gray 1997, Dayton et al. tant canopy-forming fucoids to rising temperatures
2005) and habitat loss due to coastal development and stormier seas. The mechanisms involved are dis-
(Airoldi & Beck 2007). Direct responses of biodiversity cussed and gaps in knowledge and uncertainties iden-
to global climate-driven change are superimposed tified. We speculate on the likely consequences for bio-
on these smaller-scale processes. There are growing diversity of the loss of major habitat-forming canopy
local-scale impacts due to human mitigational responses species as well as implications for the balance between
to climate change (e.g. offshore windfarms) which will primary and secondary production along wave action
increase further as tidal and wave energy schemes and latitudinal gradients. Present and future patterns
come on stream. Human adaptation to climate change and underlying processes are then placed in the con-
will also impact coastal ecosystems, particularly as text of emerging theory on the relationship between
coastal defences (Airoldi et al. 2005, Burcharth et al. biodiversity and ecosystem functioning (Hector et al.
2007) proliferate in response to rising sea levels and 1999, Loreau et al. 2002, Hooper et al. 2005, Balvanera
stormier seas (Bindoff et al. 2007). et al. 2006), derived primarily from terrestrial studies
Here we take a synoptic view of changes in intertidal (e.g. Naeem et al. 1996, Tilman et al. 2006) but also
biodiversity in response to climate change (updating aquatic systems (see Emmerson et al. 2001, Naeem
Helmuth et al. 2006) and explore the implications of 2006, Solan et al. 2006, Griffin et al. 2008). Counter to
these changes for ecosystem functioning, building on theory, increasing biodiversity of grazers is likely to be
Hawkins et al. (2008). We draw on a combination of accompanied by decreasing productivity of canopy-
published and unpublished long-term studies, model- forming algae — reasons for this apparent paradox are
ling and experiments to synthesize changes underway discussed.
in intertidal biodiversity and forecast their likely con-
sequences for ecosystem functioning. Our focus is the
intertidal zone of the North East Atlantic, particularly SPECIES DISTRIBUTIONS: PAST AND PRESENT
the British Isles and Ireland, for which there are exten-
sive historical data sets and a rich history of experi- Environmental context
mental studies (reviewed in Southward et al. 1995,
2005, Helmuth et al. 2006, Hawkins et al. 2008). Recent Fig. 1 shows the sea surface temperatures (SST)
national (e.g. Marine Environmental Change Network since 1870 at key locations around the British Isles.
and MarClim in the UK) and European networks (e.g. Those for Plymouth are shown separately for clarity, as
MarBEF LargeNet) have helped retrieve and collate most ecological data are available for this region, with
much of the data discussed below. We only consider time series stretching back 50 to 100 yr (see Southward
responses to temperature and associated environmen- 1980, Southward et al. 1995, 2005, Hawkins et al. 2003
tal variables and increased storminess for which there for reviews). These data illustrate that the western side
are reasonable predictions of future states on a 25 to of the UK is warmer than the colder waters of the North
100 yr time scale (summarised in IPCC 2007). To keep Sea and Eastern Channel (see also Sheppard 2004,
the review manageable, the impacts of reducing pH Woehrling et al. 2005). Considerable interannual and
of the oceans are not considered. Furthermore, such interdecadal variation is also shown, with warm peri-
impacts are also likely to act on a longer time scale ods (end of the 19th and beginning of the 20th century,
(50 to 100+ yr), although recent work has emphasized and the late 1950s) followed by switches to colder
that significant changes could occur much more temperatures. From the 1920s onwards, there was a
rapidly than originally anticipated, and may even be period of warming but with much fluctuation until
under way (Wootton et al. 2008). 1962, when, following the extreme winter of 1962–1963
We first outline historic fluctuations and changes (Crisp 1964), conditions were generally much cooler
in abundance and geographic distribution that are until the mid-1980s. Since 1987, conditions have be-
underway at the species level, before suggesting come much warmer, typified by milder winters due to
potential trajectories over the next 50 to 100 yr. Con- prevalence of positive North Atlantic Oscillation index
trasts are made between advancing southern species years, with predominantly westerly air flow in winter
and northern species that are likely to retreat. The across northern Europe (Mackenzie & Schiedek 2007).
species-specific nature of these changes are high- Over the last 100 yr, climate has driven major fluctua-
lighted (see also Helmuth et al. 2006). We consider tions and distributional shifts in this region (e.g. South-
 Hawkins et al.: Climate-driven ecosystem changes in Northern Europe 247

13.5
A
13
Mean annual SST (°C)

12.5
12
11.5
11
10.5
10
9.5
9
8.5
8
70

80

90

00

10

20

30

40

50

60

70

80

90

00
*
18

18

18

19

19

19

19

19

19

19

19

19

19

20
13.5 B
Fig. 1. Average yearly sea sur-
Mean annual SST (°C)

face temperature (SST) from

13.0
1870 to 2008 at (A) 4 locations
in the UK, marked on map:
12.5 Isle of Man (r), southwest Scot-
land (j), north Scotland (M) and
southeast Scotland (d); and (B)
12.0 Plymouth ( ) (note change of
*
scale to highlight fluctuations),
shown separately for clarity, as
11.5 a high proportion of long-term
Observed ecological data are from this
5 yr mean region. Data from the UK Met
11.0 Office Hadley Centre HadSST2
1870 1890 1910 1930 1950 1970 1990 2010 data set (see also Sheppard 2004,
Year Rayner et al. 2006)

ward 1980). In recent years, poleward shifts with asso- tend northwards from the Atlantic coasts of North
ciated increases in abundance of southern species and Africa and the Mediterranean, just reaching the coasts
reductions in northern species have been observed in of Britain and Ireland, while a lesser number of cold-
plankton (Beaugrand et al. 2001), fish (Beare et al. 2004, water northern boreal species have their southern dis-
Genner et al. 2004, Perry et al. 2005) and benthos tributional limits at the same latitudes (Southward &
(Hiscock et al. 2004). Phenological shifts in relation to Crisp 1954a, Crisp & Southward 1958, Lewis 1964,
climatic fluctuations have been observed in plankton Southward et al. 1995, Hiscock et al. 2004). Thus a
(Edwards & Richardson 2004) and nekton (Sims et al. boundary zone straddles the British Isles: many species
2001, 2004). Many of these changes in offshore systems reach their recorded poleward limits in the western
have been paralleled onshore, which is perhaps not English Channel between Plymouth and the Isle of
surprising given the prevalence of pelagic early life- Wight, between St. David’s Head in South Wales and
stages of most intertidal species (Southward et al. Anglesey in North Wales, on the northwest coast of Ire-
2005). Thus the intertidal zone can be considered a land or on the western and northern coasts of Scotland.
proxy for broad-scale changes in nearshore waters, Some species extend around the north of Scotland and
with the added bonus of being easy to access, inexpen- penetrate into the colder waters of the North Sea (e.g.
sive to sample and experimentally tractable, allowing Chthamalus spp., Crisp et al. 1981). There are also
explorations of underlying processes. Hence we focus some southern species which have reached northern
on intertidal systems in the present study. France but have not crossed the Channel (e.g. Haliotis
tuberculata and Gibbula pennanti). Conversely, some
northern cold water species have become very rare in
Historical patterns the south and west of Britain and Ireland, although
they can re-appear in greater abundance further south
It has long been known that numerous marine spe- in Europe in colder waters around Brittany (e.g. Alaria
cies reach their biogeographic limits around the British esculenta) and in areas with upwelling in northern
Isles (Forbes 1858). Warm-water southern species ex- Spain and Portugal (fucoid algae, Semibalanus bala-
248 Mar Ecol Prog Ser 396: 245–259, 2009

noides). There are also boreal species such as Strongy- Piette 1936, 1955). Recently, this species has pene-
locentrotus droebachiensis and the Fucus distichus trated a dispersal barrier in northern Portugal associ-
complex that have been recorded as far south as Shet- ated with relaxation of upwelling (Lima et al. 2006,
land and Orkney and the northern Scottish mainland 2007b). Algal species have expanded or contracted
(Lewis 1964, Southward et al. 1995). northwards since the 1960s (Lima et al. 2007a). South-
ern species have generally advanced poleward; the
picture is less clear for northern species, with both
Recent changes advances and retreats relative to baselines established
by surveys during the 1950s and 1960s by Ardré
Biogeographic range limits of many of the species (1971). Geographic range extensions and contractions
described above were remarkably stable over much of are likely to continue into the future. The complex
the latter half of the 20th century (Crisp & Southward topography of the British Isles, with many sea gaps (i.e.
1958, Lewis 1964, Southward et al. 1995), particularly between France and England, Ireland and Scotland)
in the region of the mid English Channel from Portland and stretches of soft coast providing barriers to disper-
Bill to the Isle of Wight. Some trimming of ranges of sal, may hinder spread of rocky shore species which
southern species did take place following mortalities could live further north (Kendall et al. 1987).
during the extremely cold winter of 1962–1963 (Crisp Similar changes have been recorded in the intertidal
1964), particularly in North Wales. During this period, and shallow subtidal zones in various other locations
some of the most striking changes were not in range around the world such as North America, Europe and
shifts, but instead changes in abundance that took Australia (see Harley et al. 2006, Helmuth et al. 2006,
place in many species, including barnacles (Southward Parmesan 2006, 2007, Poloczanska et al. 2007; for
1967, 1991) and limpets (Kendall et al. 2004). reviews, see also Ling et al. 2008, 2009). There have
Over the last decade, there have been some recent also been die-offs of intertidal (Harley 2008) and subti-
major range extensions in response to warming from dal benthos due to episodes of extreme high tempera-
the early 1990s onwards. In parallel, relative abun- tures, particularly in the Mediterranean (Coma et al.
dances of warm-water species have increased, and 2009). Furthermore, wholesale shifts in rocky reef ecol-
those of northern species have declined. Table 1 sum- ogy have been observed in the vicinity of the south-
marises these changes for key species. Southern eastern Australian climate change hotspot (after
trochids (Osilinus lineatus, Gibbula umbilicalis) have Poloczanska et al. 2007), whereby range extension of
increased in abundance and their ranges have ex- the habitat-modifying sea urchin Centrostephanus
tended in northern Scotland, Northern Ireland, North rodgersii has occurred (Ling et al. 2008).
Wales and the eastern English Channel (Mieszkowska
et al. 2007). A southern species of limpet, Patella de-
pressa, which decreased in abundance in the 1980s CHANGES WITHIN ASSEMBLAGES, AND FORE-
compared to the 1950s (Kendall et al. 2004), has largely CAST OF FUTURE COMMUNITY STATES
recovered to the levels of abundance in the previous
warm period in the 1950s. In some places it is now Most work on biological responses to climate change
much more common, although it has not re-extended has concentrated on suites of individual species rather
in great numbers beyond the Lleyn Peninsula in than on whole assemblages (but see Blight & Thompson
North Wales. Chthamalus species have increased in 2008 for work on kelp holdfast assemblages). Hence
abundance and Semibalanus balanoides has declined there is a need to anticipate broader assemblage-level
(Southward 1991). The recorded ranges of Patella impacts by drawing inference from geographic com-
ulyssiponensis, Melarhaphe neritoides and Perforatus parisons reinforced by modelling and experimentation.
(Balanus) perforatus (Herbert et al. 2003) have also ex- In particular, the role of biological interactions in model-
tended eastwards along the English Channel coast. The ling climate-driven changes is crucial to fill this gap in
most spectacular advances have been in the trochid G. understanding (Burrows & Hawkins 1998, Burrows et
umbilicalis along the English Channel coast; it now al. 2008, Poloczanska et al. 2008).
reaches Kent, an eastward extension of over 240 km. In
contrast, Chthamalus species have not breached the
barrier of the Isle of Wight (Herbert et al. 2007, 2009). Climate and competitive interactions
Further south in Europe, there has been evidence of
a northward range extension of southern species. The classic textbook example of competitive exclu-
Patella rustica was previously absent from the cold sion is the experimental work by Connell (1961) show-
upwelling region of northern Portugal and Galicia, but ing that the mid- and low-shore Semibalanus bala-
reappeared on the warmer Basque coast (e.g. Fischer- noides (then Balanus balanoides) outcompeted high
Table 1. Summary of range changes for key northern and southern rocky shore species around the British Isles and Ireland. Observations for species from further south
in Europe are included where relevant (for maps see Southward et al. 1995, updated from Helmuth et al. 2006)

Species Previous range limits New range limits Extension/retreat Comments Source

Gibbula umbilicalis North Scotland, Further east in Extension Breeding populations now present on Mieszkowska et al. (2006)
Anglesey, north Scotland the north coast of Scotland and along
Isle of Wight and north Wales the English Channel beyond the Isle
of Wight into Kent.
Osilinus (Monodonta) Lyme Regis, Spreading to Extension Isolated individuals at Portland which Mieszkowska et al. (2007)
lineatus Lleyn Peninsula Osmington, disappeared in the 1960s. Breeding
individual on populations at Osmington and isolated
Isle of Wight individuals on Isle of Wight.
Patella depressa Anglesey, Lleyn Peninsula Limited Dwindling populations on Anglesey in Kendall et al. (2004)
Isle of Wight Hayling Island re-extension the 1980s compared to 1950s have not
recovered north of Lleyn. South of Lleyn
far more common. Limited extension in
English Channel to Hayling.
Chthamalus montagui Isle of Wight, Isle of Wight, No change Both Chthamalus species are more Crisp et al. (1981),
Anglesey Wirral abundant up to range edges, but no Herbert et al. (2007, 2009),
major extensions despite suitable S. J. Hawkins (unpubl. data)
artificial habitat in English Channel.
C. montagni found along north Wales
coast to Wirral.
Chthamalus stellatus Aberdeenshire, Fife Extension Previously absent from the Isle of Man, Crisp et al. (1981),
Isle of Wight, Isle of Wight No change C. stellatus has recently been found. S. J. Hawkins (unpubl. data)
Anglesey Isle of Man Extension
Melarhaphe (Littorina) Isle of Wight, Kent Extension Now found all around the UK. Present S. J. Hawkins (unpubl. data)
neritoides Flamborough Head Yarmouth Suffolk in East Anglia on sea defences and
breakwaters.
Perforatus (Balanus) Isle of Wight Kent Extension Occurs both subtidally and on pier Herbert et al. (2003)
perforatus pilings.
Bifurcaria bifurcata Dartmouth Portland Extension Isolated populations found at Portland. Mieszkowska et al. (2006)
Clibanarius erythropus Wembury France None to date Expanded range at end of warm 1950s, Southward & Southward (1988)
eventually disappeared in late 1970s at
end of cold spell. Has not yet recolonised.
Tectura testudinalis Southern limit Limits need Retreat? No longer found on south of the Isle of Mieszkowska et al. (2006),
Irish Sea verification Man, possible retreater. Has been found S. J. Hawkins, N. Miesz-
on Anglesey and in Strangford. kowska, Brazier (unpubl. data)
Hawkins et al.: Climate-driven ecosystem changes in Northern Europe

Alaria esculenta Plymouth Lizard Point Retreat Retreated in much of the western Simkanin et al. (2005),
English Channel in the 1950s and did Mieszkowska et al. (2006)
not recolonise in the colder 1960s–1980s.
Further reduction in the abundance in
the intertidal is occurring. Reductions in
range and abundance in Ireland.
Semibalanus (Balanus) Southern limit Isolated population Retreat Reduced abundance in the UK. Major Southward (1991),
balanoides Galicia in Galicia reductions in southern limit. Wethey & Woodin (2008)

Patella vulgata Southern limit Portugal Lower on Algarve Retreat Now less common in southwest England. S. J. Hawkins (unpubl. data)
Patella ulyssiponensis Isle of Wight Beachey Head Extension Now found along south coast beyond Isle S. J. Hawkins (unpubl. data)
249

of Wight on artificial structures (Brighton

Marina) and natural substrates.
250 Mar Ecol Prog Ser 396: 245–259, 2009

shore Chthamalus montagui (then C. stellatus). Earlier, (2008) has shown that S. balanoides is virtually extinct
Southward & Crisp (1954a,b, 1956) had suggested that in Galicia (northern Spain), just persisting in a few iso-
changes in climate mediate competition between these lated locations. Under high emissions scenarios, S. bal-
species (see Wethey 1980, 1982 for similar work on S. anoides will go locally extinct more quickly, scaling up
balanoides and C. fragilis in the UK and northeast to loss over much of the coastline of south and western
USA). This work led to an extensive 40 yr time series Britain, southwest Ireland and Brittany. In estuaries, S.
(Southward 1967, 1991, Southward et al. 1995, 2005) balanoides faces competition from Elminius modestus,
encompassing 20 to 30 sites in southwest England, which was not included in the models. This Aus-
which showed fluctuations in counts of southern warm- tralasian immigrant, that arrived and established 60 yr
temperature chthamalids (C. stellatus and C. montagui ago, has locally replaced S. balanoides as the dominant
were split by Southward 1976) and the northern barnacle in areas of reduced salinity.
boreal-cold temperate S. balanoides were broadly Responses of barnacles to changing climate have
linked to temperature with a lag of 1 to 2 yr on shores also been explored with other modelling approaches.
in southwest England. Svensson et al. (2005) showed the importance of return
Southward’s data sets have been used as the basis of frequency of failure years for population dynamics of
a statistical and mechanistic modelling study by the single annual brooding Semibalanus balanoides,
Poloczanska et al. (2008) to make predictions of likely drawing on data collected in a European-scale study of
future climate scenarios on the outcomes of competi- barnacle recruitment (Jenkins et al. 2000). Coupled
tion between these species (Fig. 2). A correlative study matrix models of Chthamalus montagui (Hyder et al.
confirmed the lag of 2 yr with SST (Southward 1991), 2001) and S. balanoides populations have also been
which was used as an integrative proxy for climatic used to explore future persistence in the face of re-
conditions. This analysis also identified late spring/ cruitment variability (Svensson et al. 2006).
early summer as being the sensitive period. Moreover,
using path analysis, the direct nature of the relation-
ship of temperature with Semibalanus balanoides was Changes in fucoid canopies
highlighted; there was a highly significant negative
effect of warm weather on numbers of S. balanoides, In northern Europe, fucoids predominate on shel-
presumably acting on the vulnerable juvenile stage. In tered shores, but can extend some way out into more
contrast, there was no significant direct effect on exposed habitats (Lewis 1964). Further south they are
Chthamalus species (lumped in the analysis, but mainly more restricted to sheltered environments, with spe-
C. montagui at the high and mid-levels analysed). cies such as Fucus vesiculosus eventually only being
There was, however, a very strong negative relation- found in estuarine refuges (Ballantine 1961). In a
ship with S. balanoides, indicating an indirect effect warming world, the dynamic balance would be
due to competition. Release from competition occurred expected to shift from shores dominated by primary
in warm years. producing and shelter-providing fucoids with their
Populations were simulated using a space-limited high associated biodiversity (Thompson et al. 1996), to
model based on the work of Roughgarden et al. (1985, suspension feeder (barnacles and mussels) dominated
1994) and validated by hindcasting against the original areas with many limpets and other grazers, as in south-
time series. Various forms of the model were derived. ern Europe (Ballantine 1961, Southward et al. 1995).
A solely physically driven model simulated Semibal- This trend would be reinforced by stormier seas which
anus populations well, but Chthamalus numbers were are also predicted (Bindoff et al. 2007). Thus we have
only predicted accurately when interspecific competi- undertaken preliminary statistically based modelling
tion was included in the model. On this basis, a model studies on how changes in wave action and tem-
involving both temperature and competition was used perature should influence the distribution of canopy-
to explore low and high emissions scenarios (UK Cli- forming fucoid species.
mate Impacts Programme [UKCIP], Hulme et al. 2002). The MarClim project undertook broad-scale surveys
Even under low emissions scenarios, Semibalanus bal- of much of the coastline of the British Isles and Ireland.
anoides, the species which was dominant in the south- In parallel with this work, Burrows et al. (2008) derived
west in the 1930s (Moore & Kitching 1939) is predicted an algorithmic tool to predict wave exposure based
to become locally extinct. It is, however, likely to per- on an extension of the map-based method devised
sist in estuarine refuges and in coastal areas abutting by Thomas (1986). This can predict exposure to wave
deeper, colder water (Brittany, North Cornwall and action down to a resolution of approximately 200 m on
Land’s End; Crisp & Southward 1958) as it once did at a European scale. The MarClim data set of categorical
the extreme south of its range in Spain (Wethey & abundance of fucoids was then related to wave expo-
Woodin 2008). Recent work by Wethey & Woodin sure using a multinomial logistic regression approach.
 Hawkins et al.: Climate-driven ecosystem changes in Northern Europe 251

Model output Historical abundance S. balanoides Historical abundance Chthamalids

Physically driven Competition included in model

A 2.0
Semibalanus Semibalanus
1.8
1.6
1.4
1.2
1.0
0.8
0.6
Density (adults cm–2)

0.4
0.2
0.0
3.5
Chthamalus Chthamalus
3.0

2.5

2.0

1.5

1.0

0.5

0.0
1920 1940 1960 1980 1920 1940 1960 1980

Low emissions High emissions

B 1.6
Semibalanus Semibalanus

1.4
1.2
1
0.8
0.6
Density (adults cm–2)

0.4
0.2
0
3.5 Chthamalus Chthamalus

2.5

1.5

0.5

0
1955 1980 2005 2030 2055 2080 1955 1980 2005 2030 2055 2080
Year Year
Fig. 2. (A) Models simulating densities of the northern species Semibalanus balanoides and southern species of Chthamalus
with and without competition. These are compared against Southward’s time series (B). Using the competition-based model
which fitted best, simulations of the future under high and low emissions scenarios are shown (after Poloczanska et al. 2008)
 252 Mar Ecol Prog Ser 396: 245–259, 2009

The frequency of occurrence of shores with different Fucus canopies are known to facilitate settling barna-
categories of algal abundance was then related to cles and protect high shore sub-canopy algae (Hawkins
wave exposure and winter minimum SST. Forecasts of 1983, Leonard 2000, Ingolfsson & Hawkins 2008). Asco-
the future abundance of canopy-forming fucoid algae phyllum also facilitates a diverse algal understorey
could then be made using different scenarios of which rapidly dies once the canopy is removed (Jenkins
increasing temperature and wave action (i.e. UKCIP, et al. 1999a). Patches of F. vesiculosus provide a refuge
Hulme et al. 2002, IPCC 2007). for a diverse assemblage of invertebrates and algae
Fig. 3 illustrates how the major canopy-forming al- (Thompson et al. 1996) which would diminish if cover
gae, Ascophyllum nodosum, is forecast to respond to in- contracted. There are strong gradients of sea tempera-
creasing temperatures and wave exposure driven ture across the British Isles that can fall as low as 6°C in
by increasing wind speed. This approach has been ex- the enclosed Irish Sea and continentally influenced
tended to a suite of other canopy-forming fucoids. Table southern North Sea. Thus we forecast that temperature
2 shows the proportion of sites where Ascophyllum and rises along with increased wave action will act together
others would be ‘abundant’ (> 30% cover) on the Crisp to reduce fucoid canopy cover.
& Southward (1958) abundance scale (the other cate- The balance between fucoid algae and suspension
gories are common, frequent, occasional, rare and not feeding barnacles has long been known to be modu-
found). Fucus serratus is remarkably resilient, reflect- lated by limpet grazing (Southward 1964). Proliferation
ing its ability to occur at moderately exposed to ex- of algae occurs on more exposed shores when limpets
posed sites low on the shore. F. serratus canopies re- are experimentally removed (Jones 1948, Hawkins
duce diversity of understorey algae and invertebrates 1981, Jenkins et al. 2005, Coleman et al. 2006) or killed
due to their sweeping action (Hawkins & Harkin 1985, by oil spills and their clean up (Southward & South-
Jenkins et al. 1999b), including markedly reducing re- ward 1978). Algal growth is also high during early suc-
cruitment of barnacles (Hawkins 1983, Jenkins et al. cessional stages after placement of new structures in
1999c). Ascophyllum would appear to be surprisingly the sea (Hawkins et al. 1983, Moschella et al. 2005).
resilient, perhaps due to gradients in morphology, with Recent work has also shown that Ascophyllum is vul-
stunted short plants being able to persist in surprisingly nerable to limpet grazing (Davies et al. 2008), perhaps
exposed conditions once established. This is despite due to milder winters encouraging limpet recruitment
the known susceptibility of its germlings to wave action coupled with increased wave action. Further south in
(Miller & Vadas 1984). F. vesiculosus would be resilient Europe (Brittany), more anecdotal observations sug-
to small changes, but exhibits a sharp threshold with gest Ascophyllum is being reduced due to limpet graz-
further increases in wave action. Pelvetia would also be ing (Lorenzen 2007, S. J. Hawkins & N. Mieszkowska
expected to decrease by over 10% with modest in- pers. obs.). Such biological interactions will further com-
creases in wave action. F. spiralis appears most vulner- pound the effects of rising temperatures and increased
able, with a reduction greater than 20%. High shore wave action. Subtle behavioural and facilitative effects

A Temperature B Wave Exposure

1 Present
1 20%
Likelihood of ACFOR category

A day windier
Likelihood of ACFOR category

Present
day C
0.8 40%
0.8 F windier
O
2ºC warmer
R 0.6
0.6

0.4 0.4

0.2 0.2

0 0
6 8 10 12 0.5 1.5 2.5 3.5
February SST (°C) Wave exposure (log wave fetch)
Fig. 3. Ascophyllum nodosum. Outputs of multinomial logistic regression modelling of present day distributions versus winter sea
surface temperatures (SST; February) and wave fetch; a climate envelope model for Ascophyllum nodosum. The predicted shifts
along the ACFOR category (Abundant, Common, Frequent, Occasional and Rare) with (A) increased SST of 2°C and (B) wind
speeds of 120 and 140% are highlighted showing subsequent decreases in this key species
 Hawkins et al.: Climate-driven ecosystem changes in Northern Europe 253

Table 2. Expected percentage loss of MarClim sites where recruitment processes are ultimately responsible for
listed species are presently Abundant (> 30% cover) on the range expansions in sessile marine species, but recruit-
Crisp & Southward (1958) scale with 20 and 40% windier
ment fluctuations are also important in determining
conditions
the intensity of interactions within an assemblage of
species and hence community structure.
Species Increase in wind speed (%)
20 40 The importance of recruitment driving change is
clearly illustrated by population data for Osilinus linea-
Ascophyllum nodosum 6 11 tus (Mieszkowska et al. 2007). The range of this spe-
Fucus serratus No change No change
Fucus spiralis 21 32 cies retracted in North Wales from Anglesey to the
Fucus vesiculosus 8 20 south side of the Lleyn Peninsula in 1962–1963, follow-
Pelvetia canaliculata 11 18 ing the extremely cold winter. Subsequent recovery
and recolonisation of sites was hindered by 25 yr of
may also occur. Patella vulgata aggregates under predominantly colder weather. In recent years, O. lin-
Fucus clumps and dies or migrates when fucoid clumps eatus has breached the barrier of the Lleyn and is now
are removed (Hartnoll & Hawkins 1985, Moore et al. abundant on Anglesey, with odd individuals recruiting
2007a, Hawkins et al. 2008). This effect becomes more beyond the Great Orme ~52 km beyond previous
pronounced with increasing numbers of P. depressa, a records. In addition, range extensions of 2 chthamalid
southern species of limpet that does not aggregate species have occurred in the Irish Sea. Chthamalus
under Fucus (Moore et al. 2007a). The consequences of stellatus has extended ~77 km from the nearest popu-
P. vulgata aggregation behaviour have been modelled lations in North Wales to the Isle of Man, and C. mon-
and greater cover of fucoids persists when aggregation tagui has extensively colonised artificial structures and
occurs (Burrows & Hawkins 1998, Johnson et al. 1998). natural rock along the North Wales coast as far as the
This, along with changes in species composition of Wirral where only a single individual had been
dominant limpet grazers, has the potential to influence recorded in the 1950s by A. J. Southward (129 km, S. J.
both the dynamics and structure of shores with fucoid Hawkins pers. obs.). The range of C. montagui has also
and barnacle mosaics (Leonard 2000). extended down the east coast of Scotland ~156 km
from Aberdeen to Fife (M. T. Burrows pers. obs.). In
contrast to the case in the North Sea and Irish Sea, both
OVERVIEW AND DISCUSSION chthamalid species have failed to penetrate beyond
the Isle of Wight, despite effective reproduction right
Mechanisms driving change up to the range edges (Herbert et al. 2007, 2009).
Our work, and that by other authors, demonstrates
At range edges there are ecological limits on the that responses are species- and habitat-specific (e.g.
ability of adults to survive and reproduce, and of Lima et al. 2007a, Jones et al. 2009, Pearson et al. 2009).
propagules and larvae to reach suitable sites for suc- Together, this body of work suggests that the likelihood
cessful recruitment (Hutchins 1947). Range extensions of range extensions will be determined by a combina-
are ultimately driven by increased abundance and tion of life history traits including reproductive mode,
reproductive success of populations within the range, fecundity, larval behaviour and larval duration, all of
which provide the propagules for consistent and suc- which have the potential to influence dispersal capabil-
cessful recruitment at the range edges. This pattern ity (Gaines et al. 2007). Thus it seems unlikely that
has been recently demonstrated following the range whole assemblages will shift simultaneously, in contrast
extension of the sea urchin Centrostephanus rodgersii to plankton in very open pelagic systems (Beaugrand et
in Australia (Ling et al. 2008, 2009). Physical barriers to al. 2001). Interestingly, the greatest advances have
larval dispersal may be a proximate factor setting a been made by species such as Gibbula umbilicalis with
particular limit (Gaines et al. 2007); however, new pop- a short larval life history stage (< 3 d) and generalist
ulations at range limits also need to establish sufficient habitat requirements (Mieszkowska et al. 2006). This
numbers to overcome low density Allee effects, and species appears to have made repeated small advances
thus become self-sustaining and/or inter-connected to consolidate along the south coast of England, per-
within a meta-population network (Hughes et al. 1997). haps aided by artificial habitat provided by sea defences.
Range contractions occur when species chronically fail
to recruit or due to occasional extreme events, such as
the 1962–1963 cold winter in northern Europe (Crisp Southern advancers, northern persisters?
1964), or warm events such as have recently occurred
in the Mediterranean (Coma et al. 2009) and the Pacific Meta-analyses of a variety of marine and terrestrial
coast of North America (Harley et al. 2006). Clearly, taxa have shown that more species are advancing
254 Mar Ecol Prog Ser 396: 245–259, 2009

polewards than are retreating (Parmesan 1996, Parme- increase mortality of germlings (O’Connor & Crowe
san & Yohe 2003). Studies of intertidal species in Portu- 2005). Increased numbers of mid- to high shore Osili-
gal (Lima et al. 2007a) and the British Isles (summa- nus lineatus (Mieszkowska et al. 2007) are likely to
rized in Mieszkowska et al. 2005, Helmuth et al. 2006) impact both Fucus spiralis and Pelvetia canaliculata at
reveal a similar pattern. This could just be an artefact their lower limits, adding to mortality at their upper
of there being more southern species available to limit due to an increased frequency of extreme hot
advance from a greater diversity of clades. There may, weather events (see Schonbeck & Norton 1978, Haw-
however, be a mechanistic explanation. Where warm- kins & Hartnoll 1985). P. canaliculata and F. spiralis are
temperate and cold-temperate intertidal species co- at risk from localised extinction events at hot spots
exist, it is likely that the colder water taxon may be (Helmuth et al. 2006), which may eventually scale up
competitively superior in terms of growth rates and to whole sections of coastline.
maximum body size. This is certainly the case for bar- As juvenile and adult fucoid mortality will increase
nacles and limpets. The boreal Semibalanus bala- due to both grazing and with wave action, exposed
noides clearly grows faster and outcompetes Lusitan- shorelines become characterised by a lower density of
ian chthamalids (Southward & Crisp 1954b, Connell adult plants (Jonsson et al. 2006). Therefore, rougher
1961, Herbert et al. 2007, Poloczanska et al. 2008, seas and more frequent extreme events (Hulme et al.
Herbert et al. 2009), while Patella vulgata grows faster 2002), and greater grazer diversity as additional spe-
and outperforms P. depressa (Boaventura et al. 2002, cies are added, would be likely to reduce biomass
Moore et al. 2007b). It has been known since Thorson and production of canopy-forming macroalgae. There
(1950) that many cold-temperate and boreal species could be a shift along wave exposure gradients leading
are single brooders/spawners with reproduction linked to fewer areas dominated by large primary producers
to spring blooms (e.g. S. balanoides) or the secondary relative to those dominated by secondary producers, as
autumn peak in production (e.g. P. vulgata). This can currently occurs in southern Europe (Coleman et al.
lead to boom or bust recruitment with occasional mas- 2006). Additionally, it seems likely that fast-growing
sive recruitment events (Connell 1961, Connell et al. Semibalanus balanoides will be replaced by slower
1984, Kendall et al. 1985, Hansson et al. 2003). In con- growing chthamalid barnacles, lowering secondary
trast, southern species are often multiple brooders/ productivity of filter feeders. With fewer canopy spe-
spawners (Burrows et al. 1992) with more trickle-like cies there would be less export of algal detritus from
recruitment. Hot weather probably releases them from the system: many shores may become net importers of
competition with colder water species (Poloczanska et production from nearshore planktonic communities
al. 2008). A combination of greater competitive ability (Fig. 4, based on Hawkins et al. 1992).
and occasional massive recruitment events may ex- The British Isles and Ireland are largely surrounded
plain why northern species can still persist. However, by shallow water, and major upwelling does not occur,
several years of poor recruitment would be likely to in contrast to further south in Europe off the Portu-
lead to rapid non-linear decline of northern species guese and Spanish coasts and elsewhere in the world.
(Svensson et al. 2006), unless there are refuges such as Thus differences caused by changes in upwelling and
estuaries from which they can recolonise. recruitment regimes (e.g. Lima et al. 2006, Menge et
al. 2009) are unlikely to occur around the British Isles,
although regional-scale differences can occur due to
Implications for biodiversity and ecosystem differences in run-off and embayment influencing both
functioning nutrient status and larval retention (Burrows et al. 2009).

Warmer temperatures with associated desiccation

stress will reduce recruitment of fucoids by directly Higher biodiversity, lower production?
influencing survival, but also indirectly by suppressing
growth and reducing the likelihood of escapes The general ecological literature abounds with stud-
from grazing (Hawkins 1981, Thompson et al. 2004). ies exploring the links between biodiversity, ecological
Escapes of fucoids are more likely on dense barnacle processes and ecosystem functioning (O’Connor &
cover (Hawkins 1981). Thus switches from Semibal- Crowe 2005, Bremner 2008, Griffin et al. 2008, 2009,
anus balanoides to smaller chthamalids reduce the Maggi et al. 2009). Many single trophic level studies
probability of escapes occurring which could scale up have shown a positive relationship between assem-
from patches to whole shores (Jenkins et al. 2005). blage diversity, usually quantified as species richness,
Increases in gastropod diversity will also increase the and production using biomass as a proxy (e.g. Hector
diversity of grazing methods that are employed with et al. 1999). Together, our forecast-based statistical
habitat patches (Hawkins et al. 1989), combining to modelling and comparisons with lower latitudes in
 Hawkins et al.: Climate-driven ecosystem changes in Northern Europe 255

Exposed - barnacle dominated driven by underlying physical forcing which biological

A processes modify. Warming and increased wave action
Other carnivores
0.05? are likely to favour grazing gastropods, many of which
are from southern clades and are more diverse and
<0.01 Nucella
abundant in southern Europe (Ballantine 1961, Lewis
0.4? ? 1964, Hawkins & Hartnoll 1983, Hawkins et al. 1992,
Southward et al. 1995). Even across the British Isles,
Littorina Patella Semibalanus grazer diversity is much less in north Britain than the
? southwest (Southward et al. 1995). Grazing limpets
<0.01 75 460 also predominate numerically on more exposed shores
Microbial film Phytoplankton
in Europe (Lewis 1964, Coleman et al. 2006, Burrows
Fucoids
et al. 2009). Cooler, more sheltered conditions favour
fucoids, a northern clade. Grazers prevent establish-
ment of fucoids, but wave action primarily acts on per-
Semi-exposed - patchy Fucus-barnacle mosaics
sistence of adult plants (Jonsson et al. 2006), although
B Other carnivores adult plants can also be consumed (Davies et al. 2007).
?
Increased grazer diversity would be expected to re-
Nucella duce the probability of fucoid algae escapes given the
?
?
greater range of feeding mechanisms involved in a
? 2.5
more diverse grazer guild (Hawkins et al. 1989).
Warmer, drier weather is also likely to reduce fucoid
Littorina Patella Semibalanus
? recruitment and early survival (Thompson et al. 2004).
There may be changes in productivity in microbial
8 62 116
films with different diversity of grazers, but this re-
Fucoids Microbial film Phytoplankton mains unexplored to date and such production is likely
to be much less than that of macroalgae (Hawkins et al.
1992). Theoretically driven studies of the relationship
between biodiversity and ecosystem functioning are
C Sheltered - Fucus canopy dominated now beginning to address multitrophic interactions,
but this work is in its infancy (e.g. O’Connor & Crowe
Other carnivores
0.05? 2005, Bremner 2008, Griffin et al. 2008). More work is
needed on early stage survival of algae and inter-
3 Nucella
actions with a variety of grazers (but see Kordas &
0.2 ? 7.5 Dudgeon 2009). A combination of long-term observa-
tions with experiments and modelling should unravel
Littorina Patella Semibalanus these complex processes to turn forecasts into more
? precise predictions of future states of ecosystems, their
125 30 29 structure and ultimately their functioning.
Fucoids Microbial film Phytoplankton

Fig. 4. Major flows of energy (gC m–2 yr–1) on (A) exposed, CONCLUSIONS
barnacle-dominated shores; (B) semi-exposed, patchy Fucus –
barnacle mosaic shores; and (C) sheltered, Fucus canopy- Rapid changes are occurring in the distribution pat-
dominated shores on the Isle of Man, UK, typical of northern terns of rocky intertidal species on a European scale.
Britain where Semibalanus is the dominant mid-shore barna-
cle (adapted from Hawkins et al. 1992, Raffaelli & Hawkins
Rocky shore species can serve as cost-effective sen-
1999). Arrow width indicates relative size of energy flow. tinels for changes in nearshore ecosystems, such as in
Dotted arrows indicate interactions needing further clari- plankton and fish (Southward 1980, Southward et al.
fication. (?) Value unknown or uncertain 1995, 2005). Key organisms, such as gastropod grazers,
space-occupying barnacles and canopy-forming algae,
Europe indicates that grazer diversity is likely to make useful study taxa for predictive modelling due to
increase whilst production of canopy-forming algae is experimentally derived knowledge of ecological pro-
expected to decrease. This pattern does not match cesses that generate spatial and temporal changes in
emerging theory; there are, however, good explana- abundance. In a warming climate, the balance be-
tions for this apparent paradox. Different processes are tween grazers/suspension feeders and fucoids is likely
occurring at different trophic levels that are ultimately to alter. With the probability of algal escapes from
 256 Mar Ecol Prog Ser 396: 245–259, 2009

grazing being lower, there will be increased inter- ers (eds) Climate change 2007: the physical science basis.
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due to changes in identity and increasing diversity tributed kelp species. J Mar Biol Assoc UK 88:469–475
➤ Boaventura D, da Fonseca LC, Hawkins SJ (2002) Analysis
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Acknowledgements. S.J.H., P.J.M., M.T.B., E.P. and N.M. marine conservation and management. J Exp Mar Biol
were funded by the MarClim consortium (www.mba.ac.uk/ Ecol 366:37–47
marclim; Countryside Council for Wales, The Crown Estate, Burcharth HF, Hawkins SJ, Zanuttigh B, Lamberti A (2007)
Department for Environment and Rural Affairs, English Environmental design guidelines for low crested coastal
Nature, Environment Agency, Joint Nature Conservation structures. Elsevier, Oxford
Committee, Scottish Executive, Scottish Natural Heritage, ➤ Burrows MT, Hawkins SJ (1998) Modelling patch dynamics
States of Jersey and the Worldwide Wildlife Foundation). on rocky shores using deterministic cellular automata.
S.J.H. was also supported by NERC via a grant-in-aid funded Mar Ecol Prog Ser 167:1–13
fellowship and the Oceans 2025 programme. S.J.H. and ➤ Burrows MT, Hawkins SJ, Southward AJ (1992) A comparison
P.J.M were also supported by NERC urgency grant no. of reproduction in co-occurring chthamalid barnacles,
NE/E000029/1 and S.J.H. and S.R.J. were supported by Chthamalus stellatus (Poli) and Chthamalus montagui
NERC small grant no. NE/E010482/1. M.J.G. was supported Southward. J Exp Mar Biol Ecol 160:229–249
by a Great Western Research Fellowship. We thank all those ➤ Burrows MT, Harvey R, Robb L (2008) Wave exposure indices
who assisted with the fieldwork. H.E.S., S.J.H., N.M. and from digital coastlines and the prediction of rocky shore
S.R.J. received support from the MarBEF consortium. The late community structure. Mar Ecol Prog Ser 353:1–12
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Submitted: May 22, 2009; Accepted: October 19, 2009 Proofs received from author(s): November 30, 2009

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