Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE The rise of ochroleuca in the Western English Channel (UK) and comparisons with its competitor and assemblage dominant Dan A. Smale1,2, Thomas Wernberg2, Anna L. E. Yunnie1 & Thomas Vance3

1 Marine Biological Association of the United Kingdom, Plymouth, UK 2 UWA Oceans Institute and School of Plant Biology, University of Western Australia, Crawley, WA, Australia 3 PML Applications Ltd, Plymouth, UK

Keywords Abstract Climate change; habitat-forming species; forest; Laminariales; range expansion. The distribution of species is shifting in response to recent climate change. Changes in the abundance and distributions of habitat-forming species can have Correspondence knock-on effects on community structure, biodiversity patterns and ecological Dan A. Smale, Marine Biological Association processes. We empirically examined temporal changes in the abundance of the of the United Kingdom, The Laboratory, warm-water kelp Laminaria ochroleuca at its poleward range edge in the Wes- Citadel Hill, Plymouth PL1 2PB, UK. tern English Channel. Resurveys of historical sites indicated that the abundance E-mail: [email protected] of L. ochroleuca has increased significantly in recent decades. Moreover, exami- Accepted: 24 June 2014 nation of historical records suggested that L. ochroleuca has extended its distri- bution from sheltered coasts on to moderately wave-exposed open coasts, where doi: 10.1111/maec.12199 it now co-exists and competes with the assemblage dominant Laminaria hyper- borea. Proliferation of L. ochroleuca at its poleward range edge corresponds with a period of rapid warming in the Western English Channel. Preliminary com- parisons between L. ochroleuca and L. hyperborea highlighted some subtle but ecologically significant differences in structure and function. In summer, the average biomass of epiphytic stipe assemblages on L. hyperborea was 86 times greater than on L. ochroleuca whereas, on average, L. ochroleuca had a greater stipe length and its blade supported 18 times as many gastropod grazers (Gibbu- la cineraria). Differences in summer growth rates were also recorded, with L. ochroleuca being more productive than L. hyperborea throughout July. Com- prehensive seasonally replicated comparisons are needed to examine the wider implications of proliferation of L. ochroleuca at its poleward range edge, but our study suggests that local biodiversity patterns and ecological processes (e.g. tim- ing of productivity and trophic pathways) on shallow subtidal reefs may be altered by shifts in the relative abundances of habitat-forming kelp species.

Sunday et al. 2012; Pinsky et al. 2013; Poloczanska et al. Introduction 2013), with consequences for the structure of communi- Anthropogenic climate change has, and will continue to, ties and the functioning of entire ecosystems (Helmuth impact the Earth’s biosphere. The upper layers of the glo- et al. 2006; Hawkins et al. 2009; Doney et al. 2012). bal ocean have warmed at a rate of 0.11 °C per decade in The Northeast Atlantic region represents a hotspot of the last 40 years and, on average, have become more recent warming, as upper ocean temperatures have risen acidic, less oxygenated and experienced altered salinity at rates of ~0.3 °Cto~0.5 °C per decade (Belkin 2009; and wave regimes (Bijma et al. 2013; IPCC 2013). Hughes et al. 2010; Lima & Wethey 2012; IPCC 2013). Unequivocally, these changes in ocean climate have led to Temperatures along much of the Northeast Atlantic the redistribution of marine species (Burrows et al. 2011; coastline are predicted to increase by a further >2 °Cby

Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH 1033 Changes in NE Atlantic kelp forests Smale, Wernberg, Yunnie & Vance

2090 (Philippart et al. 2011), with major implications for magnitude), light levels (influenced by depth and turbid- marine ecosystems. Other human-derived stressors inter- ity), sedimentation, habitat type, water movement and act with regional-scale climate change in unpredictable temperature (Burrows 2012; Tuya et al. 2012; Smale et al. and non-linear ways to impact marine ecosystem struc- 2013). Even so, the dominant canopy-former along mod- ture and functioning (Russell et al. 2009; Wernberg et al. erately to fully wave-exposed coastlines across much of 2011; Russell & Connell 2012). In regions with long his- northern Europe is Laminaria hyperborea. Distributed tories of human activity, such as the Northeast Atlantic, from the Arctic to northern Portugal, L. hyperborea over-fishing, pollution and habitat alteration have (Fig. 1) can outcompete other large macroalgae under impacted nearshore ecosystems for centuries (Jackson most conditions (Hawkins & Harkin 1985). The relative et al. 2001; Airoldi & Beck 2007) and continue to interact abundance of several kelp species changes with latitude with climatic variables to induce further ecological along Northeast Atlantic coastlines, corresponding to a change. regional-scale temperature gradient, with several habitat- (large seaweeds of the order Laminariales) domi- forming kelps found at or near their range edge in the nate rocky reefs throughout the world’s temperate seas UK and Ireland (Smale et al. 2013). Because of these dis- (Steneck et al. 2002), where they provide ecosystem ser- tribution patterns, and because the distributions of some vices to humans worth billions of pounds (Beaumont inter-tidal species have shifted (Simkanin et al. 2005; et al. 2008). Kelp forests support high primary productiv- Mieszkowska et al. 2006), it has been predicted (and in ity, magnified secondary productivity and a three-dimen- some cases observed) that more southerly distributed spe- sional habitat structure for a diverse array of marine cies (e.g. Laminaria ochroleuca) will increase in abundance organisms, many of which are commercially important whereas more northerly distributed species (e.g. Alaria (Steneck et al. 2002; Smale et al. 2013). Canopy-forming esculenta) will decrease in abundance and/or undergo kelps influence their environment and other organisms, range contractions in the UK and Ireland (Breeman 1990; thereby functioning as ‘ecosystem engineers’ (sensu Jones Hiscock et al. 2004; Vance 2004; Simkanin et al. 2005; et al. 1994). By altering light levels (Wernberg et al. Brodie et al. 2009; Birchenough & Bremmer 2010). 2005), water flow (Rosman et al. 2007), physical distur- Empirical evidence for such distributional shifts and bance (Connell 2003; Smale et al. 2011) and sedimenta- appreciation of their wider implications is, however, tion rates (Eckman et al. 1989), kelps modify the local severely limited. environment for other organisms. Through direct provi- Laminaria ochroleuca is a warm-temperate Lusitanian sion of food and structural habitat, kelp forests support species, being distributed from the south of England to higher levels of biodiversity and biomass than simple, Morocco (Fig. 1), and also forming deep-water popula- unstructured habitats (Dayton 1985; Steneck et al. 2002) tions in the Mediterranean and the Azores. It is very sim- and, in general, kelp forests are hugely important as fuels ilar in morphology to L. hyperborea and is thought to for marine food webs through the capture and export of serve a similar ecological function, although relatively lit- carbon (Dayton 1985; Krumhansl & Scheibling 2012). tle is known about its ecology (with the exception of Kelps are cool-water species that are stressed by high early studies by John 1969; Drew 1974; Sheppard et al. temperatures (Steneck et al. 2002; Wernberg et al. 2013); 1978). Both species are perennial and relatively long-lived thus, seawater warming will affect the distribution, struc- (John 1969) and can form dense canopies in shallow sub- ture, productivity and resilience of kelp forests (Dayton tidal habitats. Laminaria ochroleuca was first recorded in et al. 1992; Wernberg et al. 2010; Harley et al. 2012). the far southwest of England in 1948 (Parke 1948) and Poleward range contractions of canopy-forming macroal- has subsequently progressed eastwards as far as the Isle of gae in response to oceanic warming have been predicted Wight and northwards onto Lundy Island in the Bristol (Hiscock et al. 2004; Muller et al. 2009; Raybaud et al. Channel (Blight & Thompson 2008; Brodie et al. 2009). 2013) and observed (Diez et al. 2012; Smale & Wernberg It is thought that populations on the south coast of Eng- 2013; Voerman et al. 2013) in both hemispheres. land are proliferating and that the species may be In the Northeast Atlantic, kelps occupy shallow subtid- expanding its range polewards, but evidence for this trend al reefs in all but the most sheltered or turbid locations. is largely anecdotal. Dense kelp forests are found from the lower shore to As changes in the identity and abundance of habitat- depths >20 m, from Northern Norway and Iceland forming species can have wide-ranging consequences for through to Portugal and Morocco (Hiscock 1998; Bolton community structure and ecosystem functioning (Jones 2010). The structure of entire kelp forests – in terms of et al. 1994), there is a pressing need to examine distribu- the identity and abundance of kelp species and their asso- tion shifts and their wider implications. For example, if a ciated biodiversity – varies considerably in space and time cool-water habitat-former is replaced by a warm-water as a function of wave exposure (and storm frequency and species that is functionally and structurally similar, it is

1034 Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH Smale, Wernberg, Yunnie & Vance Changes in NE Atlantic kelp forests plausible that the wider community or ecosystem will be in the abundance of Laminaria ochroleuca in the Western relatively unimpacted (e.g. Terazono et al. 2012). Con- English Channel. First, we collated presence data from a versely, if a structurally or functionally dissimilar species range of surveys and records from shallow subtidal habi- becomes dominant, or habitat formers are lost and not tats off Plymouth, UK (Fig. 1). We conducted family-, replaced, then widespread changes in biodiversity patterns genus- and species-level searches on all available statutory and ecological processes are likely to ensue (Ling 2008; data, as well as non-statutory data sets held in the Data Thomsen et al. 2010). Replacement of L. hyperborea with Archive for Seabed Species and Habitats (DASSH) and L. ochroleuca, which are similar both structurally and additional records from the National Biodiversity Net- functionally, may have relatively few knock-on effects, work (NBN). All survey data were collected at appropri- although subtle differences in kelp species traits have been ate spatial scales and quality checked; these included, for shown to influence local biodiversity patterns (Blight & example, records from Seasearch surveys and the Marine Thompson 2008). Nature Conservation Review (MNCR). Recorded This study had two objectives. First, to collate existing presences of L. ochroleuca within the study region were data and conduct additional surveys to provide a robust collated, and data collected before the year 2000 (i.e. examination of temporal trends in the distribution and 1951–1999) were compared with data collected after abundance of L. ochroleuca on the south coast of the UK. (i.e. 2000–2013). To examine possible confounding of Second, to make preliminary comparisons between sampling effort in kelp-dominated habitats between these L. ochroleuca and its competitor and assemblage domi- periods, we simultaneously analysed records for ‘all other nant in subtidal habitats, L. hyperborea, with regards to kelp species’ (i.e. Laminaria hyperborea, Laminaria digita- their morphology, physiology and ecology. ta, Saccharina latissima formerly Laminaria saccharina, Alaria esculenta). Trends in the occurrence of L. ochroleu- ca were deemed unlikely to be an artefact of sampling Methods effort, as ‘kelp’ (all other species) were recorded in 716 surveys before the year 2000 and 631 surveys afterwards, Distribution and abundance data with a similar geographical spread of sampling effort in Long-term, continuous quantitative data on the abun- both periods (Fig. 2). With regards to misidentifications dance of kelp species in shallow subtidal habitats around and reliability of the data, L. ochroleuca is conspicuous in much of the UK are lacking (Smale et al. 2013). We that (unlike other kelps) it has a light ‘golden’ coloured adopted a three-pronged approach to assess recent trends area of tissue at the basal end of the blade and the stipe

a b

c

Fig. 1. (a) The approximate distribution of Laminaria hyperborea (black line) and Laminaria ochroleuca (grey line) along the Northeast Atlantic coastline. The study region (b) and location of the study sites (c) are also shown.

Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH 1035 Changes in NE Atlantic kelp forests Smale, Wernberg, Yunnie & Vance

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Fig. 2. Records of Laminaria ochroleuca (black stars) and all other kelp species (open circles) along the south coast of Devon, UK. Records are shown for all surveys completed before the year 2000 (a) and all those completed during or after the year 2000 (b). is smooth and generally devoid of epiphytes. Juvenile sporophytes of Laminaria ochroleuca and Laminaria hy- sporophytes, however, can be difficult to distinguish from perborea at our study site off the western face of the L. digitata and L. hyperborea. As such, any ambiguous Mewstone (Fig. 1). For morphology, 10 adult plants were records (i.e. Laminaria cf. ochroleuca, Laminaria sp.) or randomly collected for each species, returned to the labo- records of juveniles were not included in the analysis. ratory and measured. For associated flora, 18 individuals Second, we selected a historical study site that was quan- of each species were harvested (the same individuals used titatively surveyed as part of a monitoring report for the for the growth assay, see below) and returned to the labo- UK Marine Special Areas of Conservation project in Sep- ratory where all epiphytes were carefully removed from tember 1999 (Moore 2000). At ~9 m depth (below chart the stipes and weighed (wet weight). Associated gastro- datum) at Duke Rock (50°20018″ N, 04°08010″ W, Fig. 1), pod grazers, found on the stipes and blades of the two Moore (2000) quantified benthic assemblages within 0.25- kelp species, were examined in situ. The occurrence of m2 quadrats (n = 22) positioned along a 16-m transect. In the blue-rayed limpet Patella pellucida and the occurrence September 2013, 14 years after the original survey, we relo- and abundance of the top shell Gibbula cineraria were cated the same subtidal reef and surveyed 0.25-m2 quadrats recorded for 10 individuals of each species. For the (n = 20) along the same transect length and bearing. As growth experiment, the ‘hole punch method’ described with the original survey, the abundance of all kelp species by Mann & Kirkman (1981) was employed, in which a was recorded in situ. Finally, we conducted detailed surveys perforation was made 5 cm from the meristem at the of kelp bed structure on a moderately exposed subtidal reef junction between the stipe and blade. In early July 2013, (west of the Mewstone, 50°18029″ N, 04°06033″ W, Fig. 1). 20 individuals of both L. ochroleuca and L. hyperborea The presence of L. ochroleuca in moderately exposed con- were hole-punched and tagged with florescent rubber ditions in the Plymouth Sound region (i.e. outside of the tubing to assist relocation (loosely cable-tied around the Breakwater, Fig. 1) was first recorded in the early 2000s, stipe). After 34 days, tagged individuals were collected yet it is now common along the moderately sheltered faces (n = 19 for L. ochroleuca and 18 for L. hyperborea) and of the Mewstone (authors’ personal observations 2012 returned to the laboratory, where the distance between onwards). At 5–7 m depth we completed 10-m-long belt the hole and the stipe-blade junction was re-measured. transects (n = 6), recording the abundances of all kelp spe- Starting at the stipe–blade junction, each kelp blade was cies within 0.5 m of each side of the transect tape (total sliced into 3-cm sections perpendicular to the direction sampling area per transect = 10 m2). Only mature sporo- of growth and each section weighed. Productivity was cal- phytes (stipe length >20 cm) were recorded to species, as culated as biomass accumulation [g fresh weight juvenile Laminaria spp. can be difficult to distinguish from (FW)day 1] by multiplying blade extension (cmday 1) one another. Transects were randomly positioned and ori- with the biomass of the heaviest of the four first thallus entated, and were at least 10 m apart. Surveys were com- sections (g FWcm 1) (see de Bettignies et al. 2013 for pleted in August and September 2013. further details and application of the method).

Morphology, physiology and ecology Statistical analysis We compared the morphology, associated flora and The Duke Rock data were not comparable to the Mew- fauna, growth and photosynthetic performance of mature stone data sets and were analysed separately. For Duke

1036 Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH Smale, Wernberg, Yunnie & Vance Changes in NE Atlantic kelp forests

Rock, comparisons between years (i.e. abundances of sedimentation, supported a very mixed kelp stand, with Laminaria hyperborea and Laminaria ochroleuca in 1999 four species contributing to the canopy (Fig. 3b). Lami- compared with 2013) were conducted with one-way per- naria ochroleuca was the second most abundant kelp spe- mutational ANOVA (Anderson 2001), using the PERMA- cies, averaging ~2 indsm 2, behind L. hyperborea, which NOVA add-on to PRIMER 6.0 (Clarke & Warwick 2001; was the assemblage dominant at densities of >5 indsm 2 Anderson et al. 2008). Similarly, response variables at the (Fig. 3b). Laminaria ochroleuca and L. hyperborea were Mewstone (i.e. differences in epiphyte biomass, grazer interspersed at the Mewstone and formed mixed canopies abundance and productivity between L. ochroleuca and (Fig. 4). Saccharina latissima and Saccorhiza polyschides L. hyperborea) were also examined with one-way permu- (order Tilopteridales not Laminariales but an important tational ANOVA. In all cases, permutations were based canopy-former) were also common (Fig. 3b). on a similarity matrix constructed from Euclidean dis- Laminaria ochroleuca and L. hyperborea populations tances between untransformed data. Permutations (999) found under the moderately wave-exposed conditions of were unrestricted and significance was accepted at the West Mewstone site are similar in morphology P < 0.05. Plots show mean values SE. (Fig. 5). There are, however, two key differences in plant structure; (i) the average stipe length of L. ochroleuca was 26% greater than that of L. hyperborea, and (ii) the stipes Results of L. ochroleuca are almost entirely devoid of epiphytes, Survey data indicated that there were more recorded in stark contrast to those of L. hyperborea (Figs 4–6). The presences of Laminaria ochroleuca in shallow subtidal mean biomass of epiphytes on L. hyperborea stipes was 86 habitats off Plymouth since 2000, compared with preced- times greater than on L. ochroleuca stipes (F1,34 = 105.44, ing years (60 records versus 32, Fig. 2). Pre-2000, L. och- P = 0.001, Fig. 6a). The epiphytic assemblage on roleuca was restricted to sheltered sites, such as inside the L. hyperborea was well developed, consisting of (amongst Plymouth breakwater or within Kingsbridge estuary others) Membranoptera alata, Phycodrys rubens and (Fig. 2). Post-2000, however, L. ochroleuca was recorded Delesseria sanguinea. In addition, a diverse epifauna was at moderately exposed sites, near the Mewstone, Hillsea observed on L. hyperborea stipes (but not L. ochroleuca), Point and some offshore reefs, for example (Fig. 2). Lam- which included barnacles (Verruca stroemia, Balanus cren- inaria ochroleuca was recorded within a depth range of 0 atus), hydroids (Obelia genticulata), ascidians (Distomus to ~15 m (below chart datum). The abundance of L. och- variolosus) and bryozoans (Celloporella hyalina, Electra roleuca significantly increased at Duke Rock between pilosa). The abundance of the gastropod grazer Gibbula

1999 and 2013 (F1,40 = 4.49, P = 0.04, Fig. 3a), but we cineraria was significantly higher on L. ochroleuca blades recorded no change in the abundance of Laminaria compared with L. hyperborea (F1,18 = 11.30, P = 0.003, hyperborea (F1,40 = 0.25, P = 1.00, Fig. 3a). Laminaria Fig. 6b), with mean abundance being 18 times greater. ochroleuca was the most abundant kelp species on bed- This was also reflected in the occurrence of G. cineraria, rock [~10 individuals (inds)m 2], possibly because Duke which was present on 80% of L. ochroleuca plants and Rock is sheltered from wave action by the breakwater, only 10% of L. hyperborea plants (Fig. 6c). By contrast, and the reef is subjected to relatively high sediment load- the limpet Patella pellucida was ubiquitous on both spe- ing. The reefs off the western face of the Mewstone, cies (Fig. 6d). Overall, the kelp stand at West Mewstone which is more exposed to wave action and less prone to was dominated by L. hyperborea but L. ochroleuca was

a b

Fig. 3. (a) Mean abundance of Laminaria ochroleuca and Laminaria hyperborea at Duke Rock (~9 m depth) in 1999 and in 2013 (0.25-m2 quadrats, n = 22 and 20 in 1999 and 2013, respectively). An asterisk indicates a significant difference between years (at P < 0.05). (b) Mean abundance of kelp species at 5–7 m depth at West Mewstone, Plymouth, 2013 (n = 6, 10-m2 transects). inds, individuals; S. latissima, Saccharina latissima; S. polyschides, Saccorhiza polyschides.

Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH 1037 Changes in NE Atlantic kelp forests Smale, Wernberg, Yunnie & Vance

a b

c

Fig. 4. Laminaria ochroleuca at 5–7 m depth at West Mewstone, Plymouth (a), where it forms a mixed stand with Laminaria hyperborea (b). Owing to a greater stipe length, L. ochroleuca individuals often protrude above the main canopy (c). abboth abundant and conspicuous, with larger individuals emerging from the main canopy (Fig. 4). The growth experiment showed that summer productiv- ity rates differed between L. ochroleuca and L. hyperborea (Fig. 7). Although the mean lamina weight of L. ochroleuca was significantly lower compared with L. hyperborea

(F1,35 = 29.25, P = 0.001, Fig. 7a), productivity rates dur- ing July were significantly greater (F1,35 =24.68, P = 0.001, Fig. 7b). Both species, however, exhibited low productivity rates during summer (L. hyperborea = 0.040 0.006 g FWday 1; L. ochroleuca = 0.097 0.009 g FWday 1).

Discussion Our study provides strong, empirical evidence for an increased distribution and abundance of Laminaria och- roleuca at its poleward range edge – the southwest coast of the UK – in recent decades. Since the 1980s, sea tem- peratures around the UK have increased by 0.2–0.6 °C per decade (Hughes et al. 2010), with greatest warming in the English Channel and southern North Sea. Within the current study region, sea temperatures are now about 0.8 °C above the long-term average, having undergone rapid warming over the past 20 years (Smyth et al. 2010). Fig. 5. Typical morphology of mature Laminaria ochroleuca (a) and Laminaria hyperborea (b) at 5–7 m depth at West Mewstone, Sea temperatures are influenced to some degree by the Plymouth. Average measurements (mm) were generated from 10 Atlantic Multidecadal Oscillation (AMO), which drives adult plants. Average number of linear segments per plant and low-frequency temperature variability (phases of 20– indicative epiphyte loads are also shown (see Fig. 6). 40 years) in the North Atlantic Ocean (Knight et al.

1038 Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH Smale, Wernberg, Yunnie & Vance Changes in NE Atlantic kelp forests

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Fig. 6. Flora and fauna associated with Laminaria ochroleuca (L. och.) and Laminaria hyperborea (L. hyp.)at5–7 m depth at West Mewstone, Plymouth. (a) Mean biomass [weight(g) of epiphyte per kg of kelp stipe, n = 18 mature plants, SE] of epiphytes attached to kelp stipes; (b) mean abundance of Gibbula cineraria on kelp individuals (n = 10 mature plants, SE); (c) occurrence of (c) G. cineraria and (d) Patella pellucida on kelp individuals (n = 10 mature plants, occurrence expressed as a percentage). An asterisk indicates a significant difference between species (at P < 0.05); occurrence data not testable. inds, individuals. ab surveys and resurveys of historical sites, would suggest with some confidence that L. ochroleuca has increased in abundance and expanded its distribution in the Western English Channel, most likely in response to recent seawa- ter warming. Within the framework recently proposed by Bates et al. (2014), it seems likely that L. ochroleuca is now in the ‘persistence’ stage of a range expansion in Southwest England, having passed through the ‘arrival’ (Parke 1948) and ‘population increase’ (John 1969) stages. In addition to latitudinal shifts, it is plausible that changes in the depth distribution of L. ochroleuca have occurred (in response to temperature, light, competitive Fig. 7. Mean (a) lamina weight (fresh weight, FW) and (b) release, for example), but these were not considered in productivity rates (FW) of Laminaria ochroleuca and Laminaria the current study. For example, L. ochroleuca has recently hyperborea at West Mewstone Plymouth, recorded during July 2013 been recorded at depths of >20 m in the Isles of Scilly (n = 19 and 18 for L. ochroleuca and L. hyperborea, respectively). An asterisk indicates a significant difference between species (at (Irving & Northern 2012) and may have proliferated ver- P < 0.05). tically as well as horizontally. Previous examinations of the distribution of L. ochrol- euca in Southwest England have concluded that is gener- 2006). Cool AMO phases occurred in the 1900s–1920s ally restricted to areas of low to moderate wave exposure and 1960s–1980s, and warm AMO phases in the 1930s– (John 1969; Drew 1974), such as within Plymouth Sound 1950s and from the 1990s to date (Knight et al. 2006; and other protected estuaries, or on the leeward sides of Mieszkowska et al. 2013). Since the end of the 20th cen- Isles of Scilly. In the last two decades, it appears that tury, anthropogenic climate forcing has been superim- L. ochroleuca has extended its distribution onto open posed onto longer-term variability trends, thereby coastlines, where it now forms a mixed stand with L. hy- exacerbating the warm phase (Mieszkowska et al. 2013). perborea, while also increasing in abundance in more Indeed, when Mary Parke (1948) identified the first sheltered sites, such as Duke Rock. Since the year 2000, L. ochroleuca specimen found in British waters, average for example, L. ochroleuca has been found on both the sea temperatures were ~1 °C cooler than at present seaward and leeward faces of the Mewstone, as well as on (Moore et al. 2011). Rapid warming of the Northeast several wave-exposed submerged reefs. Although L. hyper- Atlantic region since the 1980s has been associated with borea still forms monospecific stands on the most dramatic shifts in the distribution of plankton (Beau- exposed reefs in the region, it is almost certainly compet- grand et al. 2013), inter-tidal invertebrates (Mieszkowska ing with L. ochroleuca for resources (e.g. space and light) et al. 2006) and fish (Genner et al. 2004). In the current along moderately exposed coastlines. study, temporal patterns should be examined with some Although the specific ecological mechanisms underpin- caution, as historical time-series data were fairly limited. ning the population expansion of L. ochroleuca remain Even so, our ‘weight of evidence’ approach (see Bates largely unknown, it is clear that key processes influencing et al. 2014 for best practices for defining range shifts), range-edge dynamics of kelp species, such as growth, which incorporated anecdotal evidence, semi-quantitative survival and reproduction, are strongly influenced by

Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH 1039 Changes in NE Atlantic kelp forests Smale, Wernberg, Yunnie & Vance temperature (for recent studies, see Fredersdorf et al. through reduced thallus scouring of the sea bed during 2009; Pereira et al. 2011; Bartsch et al. 2013). The north- storms and altered light levels beneath the canopy (Too- ern limit of L. ochroleuca corresponds with the 10 °C hey et al. 2004). Second, the L. ochroleuca stipes exam- winter isotherm (Van den Hoek 1982), which lies off the ined here were almost entirely devoid of epibionts, southwest coast of England (Smyth et al. 2010). At tem- whereas L. hyperborea stipes support rich and abundant peratures around 10 °C, the gametophyte is infertile and epibiont assemblages (Whittick 1983; Christie et al. sporophyte growth is not competitive (Van den Hoek 2003). Epiphytes on L. hyperborea stipes represent an 1982; Izquierdo et al. 2002). In recent decades, the fre- important secondary habitat that supports high faunal quency of months where average temperatures were abundance and diversity. In Norway, for example, epi- below 10 °C has declined (Fig. 8), which may have pro- phytes on a single L. hyperborea stipe may harbour up to moted higher fecundity and survival rates and, ultimately, 80,000 invertebrates (Christie et al. 2003). This habitat facilitated population expansion. Moreover, the optimum cascade effect (Thomsen et al. 2010) facilitates a wide temperature for spore germination, gametophyte growth range of invertebrates, which, in turn, act as a food and fertility, and development of young sporophytes is source for kelp forest-associated fish species (Norderhaug between 15 and 18 °C (Izquierdo et al. 2002). As the fre- et al. 2005). As such, reduction of epiphytic habitat asso- quency of months with average sea temperatures exceed- ciated with a potential shift from L. hyperborea to L. och- ing 15 °C in the Western English Channel has increased roleuca may influence trophic interactions within the kelp in recent decades (Fig. 8), it may be that reproductive forest. Differences in the structure and ecology of the success and early sporophyte development has improved holdfast, which represents an important habitat for a during the recent warming trend. diversity of fauna, may also exist between the species, but At some open-coast sites near Plymouth, such as the fall outside the scope of the current study. Blight & Mewstone, L. ochroleuca now co-exists with L. hyperborea, Thompson (2008) compared holdfast epibionts of L. och- forming mixed stands, where they are in direct competi- roleuca and Laminaria digitata and showed that L. ochrol- tion for resources (e.g. space and light). As habitat-form- euca supported a distinct, relatively impoverished holdfast ing species, differences in the morphology, surface assemblage. It is possible that L. ochroleuca and L. hyper- structure and chemical composition of the stipe are likely borea harbour distinct holdfast assemblages, and this war- to be ecologically important for two reasons. First, owing rants further investigation. to their greater stipe length many L. ochroleuca individu- Our observations also suggest that the timing and fate als rise above the main canopy, dominated by L. hyperbo- of kelp-derived primary production may differ between rea, which may be a competitive advantage, especially at L. ochroleuca and L. hyperborea. It is well known that greater depths or highly turbid sites where ambient light peak production of L. hyperborea occurs from late winter levels are low. Moreover, a relatively greater stipe length through to spring, when stored organic material supports could influence conditions for understorey species, rapid growth of the new lamina (Kain 1979; Luning 1979). As such, our July growth measurements did not capture this peak period and productivity rates of L. hy- perborea were very low, as would be expected. By con- trast, very little is known about seasonal productivity of L. ochroleuca and there are no published data on in situ growth rates from the British Isles. Although seasonal data are needed to adequately assess species differences, our data indicate that growth strategies may differ between L. ochroleuca and L. hyperborea, as summer pro- ductivity rates for the former were significantly higher. Different Laminaria species exhibit different growth strat- egies (Luning 1979), and it could be that L. ochroleuca is more akin to L. digitata and Saccharina latissima, which continue to grow slowly throughout the summer and into autumn (Luning 1979). Furthermore, the route by which this material enters the food web may differ between the Fig. 8. The frequency of months per decade where average sea surface temperature (SST) in the Western English Channel off species, as L. ochroleuca plants supported significantly Plymouth (50–51° N, 4–5° W) was <10 °C (black bars) and >15 °C greater numbers of Gibbula cineraria, which were directly (grey bars). Data: Hadley Centre for Climate Prediction and Research consuming macroalgal tissue (as evidenced by grazing (http://www.badc.rl.ac.uk). marks). Although most kelp production enters the detri-

1040 Marine Ecology 36 (2015) 1033–1044 ª 2014 Blackwell Verlag GmbH Smale, Wernberg, Yunnie & Vance Changes in NE Atlantic kelp forests tal food web (Krumhansl & Scheibling 2011, 2012; de by a Marie Curie International Incoming Fellowship Bettignies et al. 2013), some is directly consumed and within the 7th European Community Framework Pro- differences in grazer preference and consumption rates of gramme. T.W. is supported by the Australian Research the different kelp species could alter trophic pathways. Council. Some of the field data described here were col- Variability in palatability and nutritional value amongst lected during survey work commissioned by Natural Eng- kelp species is important and requires further work. As land and we acknowledge this support. kelps make a significant contribution to coastal primary production, facilitate export of carbon from high to low References productivity systems, and fuel entire food webs, changes in the timing, quality or quantity of kelp production Airoldi L., Beck M.W. (2007) Loss, status and trends for resulting from climate-driven changes in kelp species coastal marine habitats of Europe. Oceanography and 35 – identity, abundance or productivity could have far-reach- Marine Biology Annual Review, , 345 405. ing consequences (Krumhansl & Scheibling 2012). Anderson M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26,32–46. In conclusion, we have empirically demonstrated that a Anderson M.J., Gorley R.N., Clarke K.R. (2008) Permanova+ habitat-forming species, L. ochroleuca, which has a warm- for Primer: Guide to Software and Statistical Methods. temperate distribution in the Northeast Atlantic, has PRIMER-E, Plymouth: 214 pp. increased in abundance at its poleward range edge and Bartsch I., Vogt J., Pehlke C., Hanelt D. (2013) Prevailing sea- has extended its distribution from sheltered to moderately surface temperatures inhibit summer reproduction of the exposed open coastlines. This pattern is in accordance kelp Laminaria digitata at Helgoland (North Sea). Journal of with climate change predictions and it seems likely that Phycology, 49, 1061–1073. the proliferation of L. ochroleuca is, at least in part, a Bates A.E., Pecl G.T., Frusher S., Hobday A.J., Wernberg T., response to increasing seawater temperatures in the Wes- Smale D.A., Sunday J.M., Hill N.A., Dulvy N.K., Colwell tern English Channel. However, the distributions of habi- R.K., Holbrook N.J., Fulton E.A., Slawinski D., Feng M., tat-forming kelp species are influenced by a range of Edgar G.J., Radford B.T., Thompson P.A., Watson R.A. environmental factors, and it is unlikely that increased (2014) Defining and observing stages of climate-mediated temperature is the sole driver of the observed pattern. range shifts in marine systems. Global Environmental Other interacting factors such as the amount of incident Change, 26,27–38. light (John 1969; Burrows 2012), nutrient and sediment Beaugrand G., McQuatters-Gollop A., Edwards M., Goberville input (Connell et al. 2008; Moy & Christie 2012), stormi- E. (2013) Long-term responses of North Atlantic calcifying ness (Byrnes et al. 2011) indirect effects of overfishing plankton to climate change. Nature Climate Change, 3, 263– (Ling 2008) and competitive interactions (Farrell & 267. Fletcher 2006) can influence kelp species distributions Beaumont N.J., Austen M.C., Mangi S.C., Townsend M. and require further study. The wider consequences of (2008) Economic valuation for the conservation of marine 56 – shifts in the relative abundances of habitat-forming kelp biodiversity. Marine Pollution Bulletin, , 386 396. species are largely unknown, but we have highlighted sev- Belkin I.M. (2009) Rapid warming of large marine ecosystems. 81 – eral key differences in the morphology, ecology and phys- Progress in Oceanography, , 207 213. de Bettignies T., Wernberg T., Lavery P.S., Vanderklift M.A., iology of L. ochroleuca compared with the assemblage Mohring M.B. (2013) Contrasting mechanisms of dominant, L. hyperborea. The co-existence of structurally dislodgement and erosion contribute to production of kelp similar canopy-forming kelps with both ‘cool’ and ‘warm’ detritus. Limnology and Oceanography, 58, 1680–1688. distributions raises some interesting questions concerning Bijma J., Portner€ H.-O., Yesson C., Rogers A.D. (2013) climate-mediated competition and other ecological pro- Climate change and the oceans – What does the future cesses occurring at the range edge. Further research is hold? Marine Pollution Bulletin, 74, 495–505. urgently needed to enhance understanding and improve Birchenough S., Bremmer J. (2010) Shallow and Shelf Subtidal predictions of kelp forest structure and functioning in Habitats and Ecology. MCCIP Annual Report Card 2010-11, warmer, stormier seas. MCCIP Science Review: 16. Blight A.J., Thompson R.C. (2008) Epibiont species richness Acknowledgements varies between holdfasts of a northern and southerly distributed kelp species. Journal of the Marine Biological We would like to thank Chris Johnson, Florian de Bettig- Association of the United Kingdom, 88, 469–475. nies, Sarah Dashfield and Sean McTierney, and all the Bolton J.J. (2010) The biogeography of kelps (Laminariales, staff at In Deep diving for assistance with fieldwork and Phaeophyceae): a global analysis with new insights from sample processing. Becky Seeley (MBA data team) and recent advances in molecular phylogenetics. Helgoland Keith Hiscock (MBA) assisted with Fig. 2. D.S. is funded Marine Research, 64, 263–279.

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