Current status and multidecadal biogeographical changes in rocky intertidal algal assemblages: The northern Spanish coast

Estuarine, Coastal and Shelf Science 171 (2016) 35e40

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Current status and multidecadal biogeographical changes in rocky intertidal algal assemblages: The northern Spanish coast
ndez C. Ferna Dpto. B.O.S. (Ecología), University of Oviedo, 33071 Oviedo, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 May 2015 Received in revised form 12 January 2016 Accepted 16 January 2016 Available online xxx

The biogeographic border between the Eastern and the Atlantic subregions of the Lusitanian Province situated on the west coast of Asturias (N. of Spain) has moved westwards in recent years. A comparative study, consisting in a resurvey of 20 shores sampled in 1977, covering 200 km showed a large-scale change affecting the mid and low eulittoral. Cold-temperate canopy species such as kelps (Laminaria hyperborea, Laminaria. ochroleuca and Saccorhiza polyschides), fucoids (Fucus serratus, Fucus vesiculosus and Himanthalia elongata) and Chondrus crispus have almost disappeared and replaced by warmtemperate species such as Cystoseira baccata, Cystoseira tamariscifolia, Bifurcaria bifurcata and coralline algae (Ellisolandia elongata, Lithophyllum incrustans and Mesophyllum lichenoides). The loss of canopyspecies can have consequences for the assemblage, especially in the case of fucoid-dominated assemblages. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Zonation patterns Intertidal assemblages Rocky shores Biogeographic changes N. of Spain

1. Introduction One of the consequences of the ocean warming is the retreat of many species of temperate seaweeds in both hemispheres (Wernberg et al., 2011). In the Northeast Atlantic an increase of sea surface temperature (SST) between 0.3 and 0.8
C per decade in the
n, 2012; Lima and last 25 years (Gonzalez-Taboada and Anado Whetey, 2012) has led to the declining abundance of large brown seaweeds (Lima et al., 2007; Fern
andez, 2011; Lamela-Silvarrey et al., 2012; Duarte et al., 2013, 2015; Voerman et al., 2013; Yesson et al., 2015). These species (kelps and fucoids) are coldtemperate key structural species characterizing intertidal and subtidal communities and the biogeographic regions along the Atlantic coast of Europe (Dinter, 2001; OSPAR, 2010). If there is a change in the distributional limits of some of these dominating species, changes in the biographic borders may be expected. The north coast of Spain is a rectilinear fringe approximately 1000 km long in which there is a transition between cold and warm temperate seaweed dominated assemblages (Lüning, 1990) and a differentiation between two biogeographic subregions, the Atlantic-influenced subregion and the eastern subregion (Dinter, 2001; OSPAR, 2010). The former is dominated by cold-temperate species (Laminaria hyperborea, Himanthalia elongata, Chondrus

E-mail address: [email protected]. http://dx.doi.org/10.1016/j.ecss.2016.01.026 0272-7714/© 2016 Elsevier Ltd. All rights reserved.

crispus, Fucus serratus) while the eastern is characterized by warmtemperate species such as Cystoseira baccata, Cystoseira tamariscifolia, Gelidium corneum, Bifurcaria bifurcata and Ellisolandia elongata. This difference is mainly caused by the summer upwelling affecting the Northwest coast of the Iberian Peninsula (Spain and Portugal) (Fraga, 1980, Fiuza, 1983; Botas et al., 1990). The boundary between these two subregions has been moving eastwards or westwards (Sauvageau, 1897; Miranda, 1931; FischerPiette, 1957, 1963) and changes in the sea surface temperature (SST) were used as an explanation for these shifts in species distribution (Fischer-Piettee, op. cit.). The last record for the border was ob
n and Niell (1981) and it was situated in the tained in 1977 by Anado west coast of Asturias (central north west coast of Spain) until
n et al., 2008) but, recently, range shifts in the 2000e2003 (Lobo species distribution have been detected. These changes can be summarized as a retreat of cold-temperate species and an expan
ndez and sion of warm temperate species (Fern
andez, 2011; Ferna
n, 2008; Duarte et al., 2013). The increase in SST, the inAnado crease in the height and strength of waves and a reduction in both,
n the strength and the duration of the summer upwelling (Anado
n, 2012, Borja et al., et al., 2009; Gonzalez-Taboada and Anado 2013; Ramos et al., 2015) may be the main drivers of the change. Because of the east-west orientation of the coast, most of the coastal waters of the North coast of Spain are found within a narrow latitudinal band, where any northward movement of isotherms is likely to affect species across very large areas (Wernberg

36


ndez / Estuarine, Coastal and Shelf Science 171 (2016) 35e40 C. Ferna

et al., 2011), so a large-scale change in the position of the boundary between the two above mentioned subregions is expected. In order to test this hypothesis, this work aimed to resurvey the same
n and Niell (1981) and use them as transects done in 1977 by Anado a baseline to: 1) describe the current status of the rocky shore intertidal assemblages along 400 km of coast to find the current border, 2) determine if changes in the structure of these assemblages since 1977 have occurred and, if so, 3) identify what those changes have been.

2. Materials and methods The study was conducted on the central north coast of Spain (Asturias, Fig. 1), where the boundary between cold and warmtemperate canopy-forming seaweeds was situated in the recent
n and Niell, 1981; Lüning, 1990; Lobo
n et al., 2008). past (Anado
n Twenty shores, the same surveyed between 1977 and 78 by Anado
n (1983), covering 400 km of coastline and Niell (1981) and Anado (Fig. 1) from Buelna (43
230 4800 N; 4
360 5100 W) to Arnao (43
330 2800 N; 07
010 2000 W) were re-surveyed in 2007e8.
n and Niell (1981) The sampling protocol was the same as Anado using the same marked fixed transect as in 1977. According to the zonation pattern, samples were distributed at different levels on the shore from the supralittoral to the low eulittoral. Using the height on the Lowest Astronomic Tide (L.A.T.) as the vertical scale, seven levels were sampled, four in the low eulittoral (level 1: 0.00e0.30 m above LAT, level 2: 0.30e0.70 m above LAT, level 3: 0.70e1.00 m above LAT, level 4: 1.00e1.50 m above LAT), two in the mid eulittoral (level 5: 1.50e2.50 m above LAT and level 6: 2.50e3.00 m above LAT) and one in the high eulittoral (level 7: between 3.00 and 4.5 m above LAT). Each shore was visited during spring tides in 1977 and revisited in 2007 and 2e4 random 50  50 cm plots were sampled in each level. The collecting technique was the complete removal of plants and associated fauna. The only exception was level 7 that was sampled using percentage cover by two main reasons: 1) to preserve Pelvetia canaliculata in those shores where it was present, due to its difficulty to recover after harvesting (Lamela-Silvarrey et al., 2012), and 2) because the

difficulties to remove crustose species like Verrucaria and barnacles. The higher levels (6 and 7) were only sampled on shores 20, 16, 11, 7 and 5, because the rest of shores are characterized by rocky cliffs and the substratum belonging to levels 6 and 7 are shingle. Apart from the fixed transects, a complete survey of each shore was done in order to provide a complete description of the zonation pattern. Samples were analyzed the same day of collection and laboratory work consisted of separation and identification of the species. Then, they were dried (60
C, 48 h) and weighted to the nearest 0.01 g. Species taxonomy was updated using Guiry and Guiry (2014) (AlgaeBase, http://www.algaebase.org) and World Register of Marine Species (WoRMS, 2014, http://www.marinespecies.org), for seaweeds, lichens and fauna.

2.1. Data analysis Vertical patterns of zonation for 5 selected shores were compared with those described in 1977, using the height on the Lowest Astronomic Tide (L.A.T.) as the vertical scale. Quantitative data on species abundance and distribution were analyzed using multivariate ordination methods on the selected subset of species and the complete set of shores. The replicate quadrats sampled in each shore level were averaged prior to multidimensional analysis. Then, the similarity of macroalgal assemblages was analyzed using non-parametric multidimensional scaling (n MDS) ordination and the Bray-Curtis coefficient as similarity index (Clarke and Green, 1988; Clarke, 1993). The multivariate analyses were performed using PRIMER for Windows v.6.0 on standardized square-root transformed data of biomass. One-way analysis of similarity (ANOSIM, Clarke, 1993) was used to test for differences between years. The contribution of each species to the observed dissimilarity between years was estimated using the similarity percentages procedure (SIMPER, Clarke, 1993). Finally, a species analysis was done for those shores in which the canopy species dominating the assemblage had reduced drastically or disappeared in 2007. After selecting the shores, all samples belonging to the same assemblage in 1977 were compared with the assemblages in 2007. Mean values of biomass (g. d. w/m2), number of species and diversity (ShannoneWiener index, H' lg2) were used as structure descriptors of the assemblage.

3. Results 3.1. Patterns of zonation

Fig. 1. The North coast of Spain and the situation of the studied shores. (1: Buelna, 2: Llanes, 3: San Antolín, 4: Ribadesella, 5: Caravia 6: La Griega, 7: Rodiles, 8: Playa ~ a, 9: Pen ~ arrubia, 10: Luanco, 11: Ban ~ ugues, 12: Verdicio, 13: Sta. María del Mar, Espan 14: Concha de Artedo, 15: Cadavedo, 16: Cueva, 17: Barayo, 18: Cartavio, 19: Punta Arenales, 20: Arnao). The main arrow shows the biogeographic border in 1977 and the ~ as as the limit of the influence of the second indicates the situation of Cape Pen summer upwelling.

Strong differences appear when comparing the zonation patterns from 1977 to 2007. For this purpose 5 shores were selected and the vertical distributions of the main assemblages according to their position on the lowest astronomic tide (LAT) are shown in Fig. 2. The main differences affect those assemblages dominated by large brown cold-temperate seaweeds: Pelvetia canaliculata, Fucus spiralis, Fucus vesiculosus, F. serratus, Himanthalia elongata, L. hyperborea, the cold-temperate red algae Chondrus crispus as well as other warm-temperate kelps (Laminaria ochroleuca, Saccorhiza polyschides). These species started to retreat since 2002 and by the time the shores were re-surveyed (2007) there were local extinctions in some shores while in others there was a marked decrease in biomass. In 2013 the canopy-forming cold-temperate seaweeds have been disappeared from most of the shores where they were dominant species in 1977 (author personal observation).


ndez / Estuarine, Coastal and Shelf Science 171 (2016) 35e40 C. Ferna

37

~ ugues (shore 11), Caravia (shore 5) and Buelna (shore 1) in 1977 and 2007. Fig. 2. Patterns of zonation at five selected localities Arnao (shore 20), Concha de Artedo (shore 14), Ban

3.2. Quantitative analysis 3.2.1. General trends in the low-eulittoral (levels 1 to 4) The MDS for all the low intertidal levels (1e4) sampled in 1977 and 2007 is shown in Fig. 3. Although the stress is 0.18, it is interpretable, and the main change is the absence of dense stands of F. serratus, Himanthalia elongata and Chondrus crispus from the western shores, especially Arnao and Punta Arenales (shores 20 and 19, respectively) in 2007. Marginal isolated populations of Chondrus crispus from shores 4, 8, 13 and 14 have also disappeared in 2007. ANOSIM analysis confirmed significant differences (R ¼ 0.238, p < 0, 01). The species which contribute to the dissimilarity between years

(Fig. 4) are Chondrus crispus, Gelidium corneum, F. serratus, and Himanthalia elongata that drastically reduce abundance while coralline algae (Ellisolandia elongata, Jania rubens, Lithophyllum incrustans and Mesophyllum lichenoides), Stypocaulon scoparia and Cystoseira tamariscifolia increase in biomass. There was no significant difference between 1977 and 2007 in terms of total biomass with the exception of Arnao (shore 20, the most western shore) due to the complete disappearance of the fucoid cover. Diversity also shows the same pattern but the pattern of variation in the number of species was different, with an increase in the western shores, especially in those in which the dominant fucoids have disappeared. The species responsible for this increase were turf species associated to articulated coralline and sand, for

2D Stress: 0,18

12 7

13

11

8 17

20

14

16

12 17

18 19 16

4 13

8

14

615 5 3 1 615 1 19 57 4

11

3

18

20

Fig. 3. MDS ordination of BrayeCurtis similarity matrix of species abundance data (square root transformed) for the low-eulittoral (levels 1 to 4). Shore numbers are indicated (cf. Fig. 1). 1977 :2007.

Fig. 4. Biomass changes (expressed as % of increase or decrease from 1977 values) of the main species contributing to the average dissimilarity (in brackets) between 1977 and 2007 according with the SIMPER routine. Black bars: cold-temperate species, grey bars: warm-temperate species.

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ndez / Estuarine, Coastal and Shelf Science 171 (2016) 35e40 C. Ferna

example several species of Ceramiales and other small Rhodophyta and Ochrophyta. 3.2.2. The low eulittoral between 0 and 0. 30 m. above L.A.T. (Levels 1 and 2) The space dominated by Chondrus crispus in 1977 has been colonized by Cystoseira baccata, Sargassum muticum, Stypocaulon scoparium and turfs in 2007 with a significant decrease in biomass (Fig. 5). The number of species also decreased (20 species in 1977 vs 13 in 2007) while diversity increased due to loss of dominance (Shannon index 1.92 vs 2.21). 3.2.3. The low eulittoral between 0. 30 and 0. 7 m. above L.A.T. (Level 2) This level, characterized in 1977 by the dominance of Himanthalia (Fig. 6) changed into a new assemblage dominated by Ellisolandia elongata and turf species (Jania rubens, Dyctiota dichotoma, Gelidium pusillum, Caulacanthus ustullatus, Mesophyllum lichenoides Osmundea pinnatifida, Boergenesiella thuyoides, Polysihonia spp., Colpomenia peregrina, Sphacelaria spp. and several species of Ceramiales). As in level 1, there is a reduction in biomass (Fig. 6) as well as in species richness (15 species in 1977 emean values-vs 12 in 2007) and a slight increase in diversity (1.93 vs 0.62).

Fig. 6. Mean biomass (g dry weight/2500 cm2) of the main species characterizing the assemblage of the level 2 in 1977 and 2007. Bars indicate S.D. Shores considered were 20, 19 and 18.

3.2.4. The low eulittoral between 0. 7 and 1. 0 m. above L.A.T. (Level 3) The F. serratus assemblage (Fig. 7) is replaced by a mixture of Bifurcaria bifurcata, Ellisolandia elongata, Stypocaulon scoparium and turf species between 1977 and 2007. Like the lowest levels described above, the same trend in biomass was observed. Diversity increased from 1,63 to 2,30 in 2007 but there was no change in the mean number of species (8 species, mean values). 3.2.5. The low eulittoral between 1. 2 and 1. 5 m. above L.A.T. (Level 4) This level is an assemblage of red calcareous algae and turfs of several species of filamentous, foliose and corticated macrophytes. Ellisolandia. elongata and Lithophyllum incrustans were the dominant species in most of the shores. There was no difference between western and eastern shores in 1977. This pattern was consistent all along the coast in both years. 3.3. The mid eulittoral (between 1. 50 and 3. 00 m above LAT)

Fig. 7. Mean biomass (g dry weight/2500 cm2) of the main species characterizing the assemblage of the level 3 in 1977 and 2007. Bars indicate S.D. Shores considered were 20, 19 and 18.

dominated by F. vesiculosus and F. spiralis being replaced by calcareous red algae Ellisolandia elongata and Lithophyllum incrustans, in exposed shores. In those shores in which there was a strong decline of F. vesiculosus, the main canopy species was replaced by a cover of ephemerals (Ulva spp., Lophosiphonia retabunda, Cladophora spp. and Ceramium spp.) with very low biomass

In semiexposed and sheltered shores levels 5 and 6 were

Fig. 5. Mean biomass (g dry weight/2500 cm2) of the main species characterizing the assemblage of the lowest level in 1977 and 2007. Bars indicate S.D. Shores considered were 20, 19 and 18.

Fig. 8. Mean biomass (g dry weight/2500 cm2) of the main species characterizing the assemblage of the level 5 in 1977 and 2007. Bars indicate S.D. Shores considered were: 20, 19, 18, 17, 15, 14 and 11.


ndez / Estuarine, Coastal and Shelf Science 171 (2016) 35e40 C. Ferna

(Fig. 8). In this case the mean number of species and the diversity showed the same decreasing trend as the biomass. 3.4. The high eulittoral (between 3. 00 and 4. 50 m above LAT) This level did not show changes from 1977. In exposed and semiexposed shores it is dominated by barnacles (Chthamalus montaguii and Chthamalus stellatus), trochids (Phorcus lineatus) limpets (Patella rustica) and littorinids (Melaraphe neritoides) with patches of Pelvetia canaliculata covering rocks in the inner part of semiexposed shores but forming dense stands in sheltered shores. 4. Discussion As expected, the boundary between the two biogeographic subregions described in the North coast of Spain: the west Atlanticinfluenced and the eastern (Dinter, 2001; OSPAR, 2010) has moved westwards, so all the North coast of Spain may be now considered belonging to the same subprovince, the eastern. The species responsible for this change are cold temperate canopy species dominating intertidal assemblages in the low eulittoral as L. hyperborea, Himanthalia elongata, Chondrus crispus, F. serratus and the mid eulittoral F. vesiculosus. Some of them have practically disappeared such as L. hyperborea (Fern
andez, 2011) and Himanthalia elongata (Duarte et al., 2013; Martínez et al., 2014) while others, like F. serratus, F. vesiculosus and Chondrus crispus remain in small isolated patches of individuals in poor condition (Duarte
ndez, 2011; Martínez et al., 2014). They reapet al., 2013; Ferna ~ a, in the North West pear as canopy dominant species near La Corun corner of the Iberian Peninsula (Ramos et al., 2015). Most of warm-temperate species increased their abundance at the low eulittoral as Cystoseira baccata, Cystoseira tamariscifolia, Bifurcaria bifurcata, Stypocaulon scoparium and coralline algae (Ellisolandia elongata, Lithopyllum incrustans and Mesophyllum lichenoides). But, contrary to expected, some warm-temperate kelps (L. ochroleuca and Saccorhiza polyschides) are also in retreat. While they increased in abundance in the British Isles (Smale et al., 2014), in the North coast of Spain L. ochroleuca has almost disappeared and ~ as (Ferna
ndez, 2011). The S. polyschides is absent east from Cape Pen stressful period of more than 30 consecutive days of SST> 20
C ~ as may be the respondescribed in the coastal waters of Cape Pen sible of these range shifts in kelps distribution. In the case of S. polyschides, the three stages on the range of species shifts: poor performance, population decline and local extinction (Bates et al., 2014) may be recognized in the long-series of data from the region ~ as (Ferna
ndez, 2011). Something similar may have of Cape Pen occurred in the case of L. ochroleuca and the less temperature tolerant species L. hyperborea and Himanthalia elongata that have disappeared from all the shores. In the western shores F. serratus, Chondrus crispus and Saccorhiza polyschides are at the stage of population decrease with local extinctions of C. crispus and S. polyschides in the eastern shores. The case of F. vesiculosus is another example of species-specific response to the temperature increase. Intertidal species are considered more resistant to rising temperature because they are adapted to a wider temperature range (Schonbeck and Norton, 1978) but those occurring lower in the shore such as F. vesiculosus may be the more sensitive. Among the fucoids growing on the central coast of the North of Spain, F. vesiculosus was considered the most vulnerable species to increasing temperature, according to the sharp decrease in abundance and the predicted model for stability (Lamela-Silvarrey et al., 2012). This has now disappeared from the North coast of Spain as with the above mentioned large brown seaweeds. Since the beginning of the 20th century, the North coast of Spain

39

was described as a region in which cold-temperate seaweed assemblages were replaced by warm-temperate seaweed assemblages following a west-east longitudinal gradient (Fischer-Piette, 1957). This west or eastwards movement was explained by the alternation of cold and warm periods (Fischer-Piette, 1957). Years later, the gradient was defined in terms of SST, nutrients, primary and secondary production (Lüning, 1990; Philippart et al., 2007) as a consequence of a summer upwelling affecting the north-western
~ as at the coast (Botas et al., 1990; Alvarez et al., 2010), with Cape Pen limit of the upwelling influence (Botas et al., 1990). Recent oceanographic research showed changes causing an increase in the period of stratification, a reduction in the intensity of the upwelling as well as an increasing trend in SST (Llope et al., 2007; Gonzalez
n, 2012). This relaxation in the summer upTaboada and Anado welling might be the reason for a similar shift in species distribution along the Portuguese coast (Tuya et al., 2012). The consequence of the loss of canopy-forming seaweeds is severe for the assemblage because their structural and functional role could not be easily fulfilled by other species (Crowe et al., 2013). For this reason, changes in the lowest eulittoral, where kelps were replaced by Cystoseira species, are less severe because it is just a replacement of canopy species. The habitat continues being structurally complex but probably with a considerable loss of kelpassociated species, due to the very large amount of species the stipe and holdfast of kelp contains (Edwards, 1980; Norton and Burrows, 1969). The remaining assemblages, dominated by fucoids or Chondrus crispus have experienced strong changes in structure, including the loss of architecture and habitat, as well as biomass and biodiversity. These changes especially affect the associated understorey macroalgae (Valdivia et al., 2010) and fauna (Christie et al., 2009; Duarte et al., 2015). In the low eulittoral, the shift from assemblages dominated by canopy-forming fucoids (H. elongata, F. serratus) to assemblages dominated by turfs of coralline algae is widely described in the literature (Benedetti-Cecchi and Cinelli, 1992; Connell, 2003; Díez et al., 2012.) as a consequence of changes in the resources, especially the increase in sunlight and sediment due to a loss of canopy. Large-scale changes also affect the mid-eulittoral, where dense stands of F. vesiculosus have been replaced by a cover of ephemerals. In a warming world, increases of both temperature and wave action predict a shift from shores dominated by fucoids to shores dominated by barnacles and limpets (Hawkins et al., 2009) and, from the predictive models, F. vesiculosus was considered the most vulnerable fucoid species in terms of stability and resilience (Hawkins et al., 2009; Lamela-Silvarrey et al., 2012). The loss of biomass and habitat also promote the disappearance of associated species, mainly small mesograzers as several authors have shown in other € m and latitudes (Brawley, 1992; Thompson et al., 1996; Wikstro Kautsky, 2007). The present study suggests a reinterpretation of the biogeography of the Iberian Peninsula as Tuya et al. (2012) proposed for the coast of Portugal, another transition zone in the Iberian Peninsula in which similar shifts in species distributions have been detected. Apart from the fact that along the North coast of Spain there is a gradient in biomass, species richness and diversity decreasing eastwards (Ramos et al., 2015), there is now no difference in the structure of the assemblages. Even using new tools for coastal classification (including both biological and physical variables) only the North West corner of the Spanish coast seems to be different form the rest of the Spanish Atlantic coast (Ramos et al., 2015). Since the biogeographic border separating the Atlantic-influenced region and the eastern region, situated in the western part of the
n and Niell, 1981) has disappeared, all the north coast coast (Anado of Spain may be considered as homogenous in terms of species

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ndez / Estuarine, Coastal and Shelf Science 171 (2016) 35e40 C. Ferna

assemblages and included in the eastern subregion. Acknowledgments This research was supported by the national project
n y modelizacio
n de los patrones de variacio
n “Caracterizacio espacial y temporal de las comunidades costeras de Asturias” (CTM
n for the use and infor2006-05588). I am grateful to Dr. R. Anado mation on his historical data. I also thank Dr. J. Arrontes for advice on data analysis and Dr. J.M. Rico for linguistic assistance. I also appreciate the critical review by anonymous referees. References
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