Fucoid Assemblages on the North Coast of Spain: Past and Present (1977 – 2007)

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Fucoid assemblages on the north coast of Spain: past and present (1977 – 2007)

Cristina Lamela-Silvarrey, Consolaci ó n Fern á ndez *, of the Bay of Biscay has warmer temperatures, whereas the Ricardo Anad ó n and Julio Arrontes western side has cooler waters. Summer upwelling occur- Á rea de Ecolog í a , Departamento de Biolog í a de ring every year on the northwestern Spanish coast (Fraga Organismos y Sistemas, Universidad de Oviedo, Oviedo 1981 , Botas et al. 1990 ) seems to account for this boundary. 33071 , Spain , e-mail: [email protected] Depending on upwelling intensity, this border moves west- wards/eastwards periodically (Fischer -Piette 1957 , Anad ó n * Corresponding author and Niell 1981). During the last decade, an increasing temperature trend has been recorded along the north coast of Spain – an increase of Abstract 0.55 °C occurred in oceanic waters, whereas in coastal waters, the temperature rose by 0.21° C (Llope et al. 2006 ). In addi- Fucoid assemblages dominated by Pelvetia canaliculata , tion, the intensity and duration of upwellings have decreased Fucus spiralis , F. vesiculosus, and Ascophyllum nodosum since 1968 (Lav í n et al. 2000 , Cabanas et al. 2003 , Llope et al. located at two sites on the central coast of Asturias (northern 2006 , P é rez et al. 2010 , Santos et al. 2011 ). Both processes are Spain) were sampled monthly in 1977. Repeating the same related to current climate change (Ruiz Villareal et al. 2009 ). sampling methodology, a resurvey was done in 2007 to detect Due to increased air and sea surface temperatures (SSTs), changes in the abundances of the species using the previous data as a baseline. Annual net primary production was lower there has been a poleward movement of cold water species for all the species in 2007, and there were differences in the in intertidal assemblages (Helmuth et al. 2006 , Hawkins timing of maximum biomass for P. canaliculata and F. vesic- et al. 2008, 2009 ); phenological changes in intertidal gas- ulosus, as well as a shortening of the growth period in 2007. tropods have also been reported (Moore et al. 2011 ). There Associated fauna also differed between dates. Higher abun- has been a reduction in canopy-forming brown algal species dances of Gibbula spp. occurred in 2007, whereas littorinid since the late 1990s (Sagarin et al. 1999 , Steneck et al. 2002 , species densities in the upper intertidal were reduced in that Airoldi and Beck 2007 , Fern á ndez 2011 ). year. As a result, the fucoid-grazers balance changed, with Use of historical data is a very common tool for detect- P. canaliculata and particularly F. vesiculosus , being the ing long-term changes, especially those resulting from human Q1: assemblages most sensitive to change. Observed modifi ca- activities. Even though the northeast Atlantic Coast is one of the best studied in the world, few historical quantitative data Please tions were not merely fl uctuations in the biomass patterns of confi rm the these species, but also responses to increases in air tempera- are available. The exception is a time series of zooplankton change in ture and sea surface temperature and to a shift in the frequency and intertidal invertebrates in the British Isles going back the sentence and seasonality of upwelling episodes. Other long-term abi- to the 1920s (Southward et al. 1995, 2005 , Thompson et al. “Even otic fl uctuations not directly related to global warming should 2002 , Hawkins et al. 2008, 2009 ). Elsewhere, the benchmarks though ... are available.” also be considered as possible drivers for these changes. are single historical baselines (e.g., for the Iberian Peninsula; Fischer -Piette 1955 , Fischer -Piette and Gaillard 1959 , Ardr é Keywords: fucoids; grazing; northern Spain; primary 1970, 1971 , Lima et al. 2006, 2007 ). production; seasonal patterns. This study uses the quantitative biomass data collected in 1977 on Pelvetia canaliculata (Linnaeus) Decaisne et Thuret, Fucus spiralis Linnaeus, F. vesiculosus Linnaeus, and Introduction Ascophyllum nodosum (Linnaeus) le Jolis assemblages as a baseline, to compare with data collected in 2007. Resurveying Sheltered and semi-exposed rocky shores of the Atlantic sites after a span of 30 years might prove useful, as preliminary Q2: Coast of Europe are dominated by dense canopies of fucoids information on patterns of variability of species in relation to Please clarify (Lewis 1964 ), but on the north coast of Spain and Portugal, changes in the environment though to infer causality may be the sentence these algae are restricted to sheltered shores, as warmer diffi cult due to the way the environment changes. Because “Resurveying waters favor the development of limpet and barnacle popula- years within periods were not replicated, our approach will sites ... changes” tions at the expense of seaweeds (Ballantine 1961 , Hawkins allow only detection of differences between specifi c years. and Hartnoll 1983 , Hawkins et al. 1992 ). Thus, the aims of this study were (1) to detect differences Along the north coast of Spain, the distribution of fucoid among the annual patterns of biomass and primary production species is restricted to the western sector (L ü ning 1990). of canopy-forming fucoids on sheltered shores after a 30-year This is due to a west-east thermal gradient – the eastern part time interval, and (2) to assess whether any of these changes

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2 C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain

were consistent with the changes in the coastal waters, espe- Samples were analyzed on the day of collection; laboratory Q4: cially temperature and upwelling intensity and duration. work consisted of separation and identifi cation of the species; All for the associated fauna, only gastropods were considered. mathematical Fucoid receptacle biomass and vegetative biomass were dif- variables and Materials and methods ferentiated. Seaweeds and gastropods were then dried to con- superscripts ° and stant weight (60 C, 48 h) and weighed to the nearest 0.01 g. subscripts Study site Net primary production (NPP) was estimated as the increase have been set in biomass (∆ B) at monthly intervals (Westlake 1969 , Anad ó n to roman for This study was conducted at two localities on the north coast of and Fern á ndez 1984 ): consistency, Spain: Ba ñ ugues (43° 37 ′ N, 5° 38 ′ W) and El Puntal (43° 32 ′ N, if you would ° ′ = Σ∆ Σ∆ prefer in 5 23 W). Pi Bi + Br Ba ñ ugues is a shore comprising a heterogeneous wave-cut italic please where B is the biomass of the main species, and B is the indicate rock platform with many large blocks and boulders semi- i r clearly where exposed to wave action (Arrontes 1990 ). Pelvetia canali- biomass of the remaining species. The balance between fucoid algae and grazers was exam- it should culata , Fucus spiralis, and F. vesiculosus were the dominant ined by adjusting our data to make use of the model proposed be applied. fucoids in the sheltered sites from upper to mid-shore. For Please by Noy-Meir (1975) for grazing systems; this procedure more details regarding the Bañ ugues zonation pattern, see confi rm examines the stability or instability of the system in question. Ferná ndez and Niell (1982). El Puntal is a very sheltered NPP, and mean and maximum algal biomass were used to cal- shore at the mouth of the Rí a of Villaviciosa with a mixture culate plant isoclines. V is the biomass at which growth is of sandy patches and rock boulders; Ascophyllum nodosum is x maximum, and it was estimated as the balance between NPP the main fucoid covering rocks and stones. and mean biomass; Vm is the maximum biomass in ungrazed vegetation. Data for herbivore isoclines were theoretical Q5: Temperature data postulates because there were insuffi cient empirical data for Please supply complete Surface seawater temperature (SST) data recorded closest grazers. Q3: Algal and faunal species taxonomy were updated using date when Please spell to Ba ñ ugues (43 ° 62 ′ N, 5° 65 ′ W) were obtained by AVHRR the site was Guiry and Guiry (2010) (AlgaeBase, accessed on XX June, out ‘AVHRR’ sensors from the satellites NOAA-12 to NOAA-18 (Reynolds accessed. See if appropriate et al. 2007 ). 2010 at http://www.algaebase.org) and Appeltans et al. (2010) also Guiry and not [World Register of Marine Species (WoRMS), accessed on and Guiry (2010) and generally Biological data XX June, 2010 at http://www.marinespecies.org]. known to the Appeltans et readership al. (2010) Two sets of biomass data were considered: data from 1977 Statistical analysis were compiled from an academic report (Anad ó n 1980 ), and Temporal changes in abundance patterns of fucoid assem- data for 2007 were collected monthly (bimonthly in the case blages at Ba ñ ugues and El Puntal were analyzed using analy- of A. nodosum ) during a complete year following the same sis of variance (ANOVA). Two factors were defi ned: methodology. Data collected in 1981 and 1984 for F. vesiculosus were also considered (Arrontes 1983, 1987 ) (see Table • Season (S): Season was considered a fi xed factor with 1 for additional details). two levels (winter and summer). Each season had three The collecting technique involved complete removal of all replicates corresponding to the sampling date of the three algae and associated fauna in two to three randomly chosen months included in each season (i.e., winter comprised data plots of 50 × 50 cm (30 × 30 cm in the case of P. canaliculata ). for December, January, and February; summer comprised

Table 1 Details of localities, assemblages analyzed, and data compiled for the study.

Localities Year Sampling periods Samples Zone Source per month

Ba ñ ugues 1977 November 1976 to October 1977 2 Pelvetia canaliculata A n a d ó n , 1 9 8 0 Gonz á lez and Anad ó n, 1981 1 Fucus spiralis 1 Fucus vesiculosus 1981 June 1981 to May 1982 2 Fucus vesiculosus Arrontes , 1983 1984 July 1984 to November 1985a 2 Fucus vesiculosus Arrontes, 1987 2007 October 2007 to September 2008 2 Pelvetia canaliculata Present study Fucus spiralis Fucus vesiculosus El Puntal 1977 November 1976 to October 1977 1 Ascophyllum nodosum Anadó n, 1980 2007 October 2007 to August 2008 2 Ascophyllum nodosum This study a Only data from July 1984 to June 1985 were considered. Article in press - uncorrected proof

C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain 3

data for June, July, and August). In the case of A. nodo- There was a similar trend in the Fucus vesiculosus annual sum, only two replicates per season were considered due cycle. Biomass peaked in the summers of 1977, 1981, and to the shortage of samples. As A. nodosum , F. spiralis , and 1984, and in mid-late spring in 2007 (Figure 2 B). In contrast, F. vesiculosus assemblages had only one sample per month two annual biomass cycles occurred during the 1980s (1981, in certain years, only one sample per month was considered 1984); only 1981 is presented here in the fi gures because no in order to balance sample sizes between years. For P. canali- signifi cant differences between years were observed, and culata , an average of two samples per month was used. receptacle biomass data were available only for 1981. Means • Year (Y): Year was considered a fi xed factor with two lev- for 1977 and 1981 were signifi cantly different and so were els (1977, 2007), except for F. vesiculosus , for which year the differences between seasons (Table 2 ). Fucus vesiculo- had three levels (1977, 1984, and 2007). sus receptacle biomass decreased from 1981 to 2007 (Figure 2 B). Q6: ‘OS’ Analysis was performed by using the statistical package In the case of F. spiralis, the pattern of biomass was not dif- has been STATISTICA 8 (StatSoft, Tulsa, OK, USA) for Microsoft ferent between 1977 and 2007 – the period of growth occurred expanded. Windows operating system. Transformations of algal biomass Abbrevia- from spring through autumn and there were signifi cant differ- data were not necessary; Cochran’ s C test was applied to test tions/ ences between winter and summer (Table 2 ). However, values for homoscedasticity. A post hoc Tukey test was applied only acronyms in 1977 were signifi cantly lower (Figure 2 C, Table 2 ), as 2007 in the case of P. canaliculata , as there were more than three mentioned had a greater peak of biomass in mid-late spring and another only once levels in the Y (year) × S (season) interaction: 1977 winter, one smaller peak in autumn. Receptacle biomass was low in do not 1977 summer, 2007 winter, and 2007 summer. need to be winter, with a sharp increase in spring, a peak in summer, and abbreviated a decline in mid-autumn (Figure 2 C). The growing period of Results Ascophyllum nodosum in 1977 began in March and fi nished in October, whereas in 2007, growth occurred from April to Temperature data August (Figure 2 D); only differences between years were signifi cant (Table 2 ). There have been increases in SST and air temperature over All the species had lower NPP values in 2007 than in 1977 recent decades. Since the mid-1980s, both SST mean and (Table 3 ), probably due to the reduction in the lengths of maximum values have risen (Figure 1 A,B), especially the growing periods (Figure 2 ). However, average biomass since 1993. Air temperature also increased for the period changed differently among species – F. spiralis and A. nodo- 1970 – 2009, especially in summer (0.40 ° /decade; Gonzá lez- sum biomasses increased (Table 3 ), that of P. canaliculata Taboada and Anad ó n-Alvarez 2011 ). decreased, and there was no clear trend for F. vesiculosus (Table 3 ). Fucoid species Gastropoda Pelvetia canaliculata had a growing period spanning winter through summer with a maximum in August in 1977, Annual and seasonal changes for only the most abundant spe- whereas in 2007, the period shortened to spring, with a maxi- cies are presented. A list of gastropod species present in each mum in May (Figure 2 A). For this species, there was a sig- assemblage during 1977, 1981, and 2007 is given in Table 4. nifi cant interaction between year and season (Table 2, Figure Fauna associated with the P. canaliculata assemblage was 3 ). Biomass values recorded in the summer of 2007 were dominated by littorinids, of which Melarhaphe neritoides the lowest, whereas those from summer of 1977 were the (Linnaeus 1758) was the most abundant species. Differences highest (Figure 3 ). Receptacles were present all year; from in the timing of density peaks occurred between 1977 and March to July, their biomass represented ≥ 50% of the total 2007 – maximum values were recorded in spring (April) (Figure 2 A). and early summer (June and July) in 1977, whereas in 2007,

Figure 1 (A) Mean annual SST and (B) maximum annual SST (from 1985 to 2006). Dashed lines show the ﬁ tted regression lines y = 0.018*x-20.590, R2 = 0.137 (A) and y = 052*x-82.128, R 2 = 0.279 (B). Article in press - uncorrected proof

4 C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain

Figure 2 Annual biomass pattern of (A) Pelvetia canaliculata, (B) Fucus vesiculosus, (C) F. spiralis, and (D) Ascophyllum nodosum in 1977, 1981 (for F. vesiculosus only), and 2007. Where data exist, receptacle biomass is also shown (fi lled areas). Data include single monthly values and monthly means with standard devia- tion bars (n = 2 for A. nodosum ; n = 3 for the other species); these bars are not shown for receptacle biomass in order to reduce fi gure complex- ity. Two annual biomass cycles of F. vesiculosus were tracked in 1981 and 1984, showing no signifi cant differences between them (ANOVA, p > 0.05), and only data for 1981 are presented. DW, dry weight.

Table 2 ANOVA testing the effects of year (1977, 1981, and 2007), season (winter and summer), and their interaction on species abundance.

Source Pelvetia canaliculata Fucus spiralis df MS F p-Value df MS F p-Value

Year 1 1111.92 7.780.024 1 2 4 3 3 . 2 1 . 6 3 0 . 2 3 7 Season 1 2199.49 15.400.004 119,897.413.35 0.006 Y × S11487.6810.410.012 1 4 6 8 8 . 4 3 . 1 5 0 . 1 1 4 Error 8 142.86 8 1490.5 Fucus vesiculosus Ascophyllum nodosum Q7: df MS F p-Value df MS F p-Value ≤ Please Year 2 56,644 19.05 0.001 1 7 8 , 7 4 7 4 . 9 0 0 . 0 9 1 ≤ conﬁ rm Season 1 120,090 40.39 0.001 1279,86517.41 0.014 × additional Y S 2 1 1 9 0 . 0 4 0 . 9 6 1 1 1 7 3 3 0 . 1 1 0 . 7 5 9 data for Error 122973 4 116,078 Table 2 Statistically signiﬁ cant values (p ≤ 0.05) are shown in bold. df, degrees of freedom; MS, mean square.

peaks occurred in spring (April), autumn (October), and assemblage at very low densities and were not included in winter (January) (Figure 4 A), but there were no signiﬁ cant the analyses. differences in density. Another important species, Littorina Melarhaphe neritoides and L. obtusata were also found at obtusata (Linnaeus 1758), was present year-round in 1977, high densities in F. spiralis assemblage in 2007. Melarhaphe with maximum values in winter, whereas in 2007, it was neritoides , which was not detected in 1977, was present in only observed during spring (Figure 4 B). Limpets (Patella winter and spring, with high densities close to 3000 individu- spp.) and trochids ( Gibbula spp.) were also present in this als m -2 in winter. Similarly, L. obtusata was not present during Article in press - uncorrected proof

C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain 5

wave exposure, nutrient availability, and temperature). In addition to this, the seasonality of conditions in mid- latitude habitats drives seasonal patterns of growth and reproduction in these macroalgae (Chapman 1995 ). In the northeastern Atlantic, along the European shores, fronds of Pelvetia canaliculata, Fucus spiralis, F. vesiculosus , and Ascophyllum nodosum grow from the end of winter to mid-summer, reproduce in summer, and become senescent at the end of this season. In autumn, fronds are pruned back and new fronds arise from the holdfast in winter (Little and Kitching 1996 ). This general pattern varies slightly between northern and southern populations (i.e., British Isles and Brittany vs. northern Spain and Portugal; Knight and Parke 1950 , Fischer-Piette 1959, Subrahmanyan 1960, 1961, Ardré 1970); reproduction begins earlier in southern populations (Fischer-Piette 1959, Ardré 1971). Data collected in 1977 on the north coast of Spain fit with these general trends; however, 30 years later (2007), some Figure 3 Results of post hoc Tukey test for Pelvetia canaliculata changes were detected – NPP had diminished in all the biomass. a, b indicate the different group means in the test at p < 0.05. w, winter; s, summer. assemblages and, in those dominated by P. canaliculata and F. vesiculosus, there was a shortening of the growth period. As a consequence, the peak of biomass of both species shifted to spring. Q8: the summer season of 1977, but reached high-density values Fucoids in the uppermost intertidal, such as P. canalicu- There should during this period in 2007 (Figure 4 C). Greater densities of lata, have a physiological fl exibility enabling them to sur- be one F Gibbula spp. also occurred in 2007, especially during the late vive in sites under short- and long-term fl uctuations in air value and 2 spring-early summer period (Figure 4 D). exposure (Schonbeck and Norton 1979 ). However, these degrees of The main gastropod species in the F. vesiculosus assem- physiological limits can be exceeded during extreme events, freedom (one especially in hot summers during neap tides, leading to die of which blage was L. obtusata , with lower densities in 1977 and off at the tops of the zone (Schonbeck and Norton 1978 , should be 1 2007 than in 1981 (Figure 4 E). One-way ANOVA with log- because you transformed data showed signifi cant differences among years Hawkins and Hartnoll 1985 ). In recent years in Asturias, compare 2 (F = 36.77, p < 0.001, SNK 1981 > 1977 = 2007). Gibbula spp. there has been a trend of increasing temperatures – especially years). Please were extremely rare in 1977, but occurred year-round and in summer – and in increments of the number of days with check and reached higher densities in 2007 (Figure 4 F). air temperatures ≥ 20 ° C (Gonz á lez-Taboada and Anad ó n- confi rm In the A. nodosum assemblage, limpets and trochids were Alvarez 2011). Although these temperatures cannot be con- Q9: the most abundant gastropod species, whereas L. obtusata sidered lethal, sublethal effects may prevent the growth and Please spell was scarce. As in F. spiralis and F. vesiculosus assemblages, reproduction of a species (Schonbeck and Norton 1978 , out ‘SNK’ if Gibbula spp. increased in number between 1977 and 2007 Thompson et al. 2002 ), especially if these conditions persist appropriate over several days. and not (Figure 4 G). generally Changes in nutrient availability and water temperature known to the may have been additional factors determining differences readership Discussion between 1977 and 2007. In summer, nutrient-rich, cool upwelling water brings suitable conditions for settlement Fucoids are adapted to highly variable environmental and development of north-temperate species in the western conditions characteristic of intertidal environments (e.g., part of the Bay of Biscay (L ü ning 1990). Thus, the changes

Table 3 NPP and annual average biomass of Pelvetia canaliculata, Fucus spiralis, Fucus vesiculosus, and Ascophyllum nodosum assemblages.

Species NPP (g DW m-2 year-1 ) Annual average biomass (g DW m-2 ) 1977 1981 2007 1977 1981 2007

Pelvetia canaliculata 1274.52 1170.11 1023.70 788.73 Fucus spiralis 1 0 5 2 . 6 6 8 5 7 . 2 8 6 6 7 . 1 8 8 3 3 . 6 2 Fucus vesiculosus 2255.01 1511.88 1431.80 1111.08 1564.54 950.47 Ascophyllum nodosum 3115.87 2455.24 2581.70 3181.13 DW, dry weight. Article in press - uncorrected proof

6 C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain

Table 4 Gastropod species present in Pelvetia canaliculata, Fucus spiralis, Fucus vesiculosus, and Ascophyllum nodosum assemblages.

Species Assemblage* PC FS FV AN 77 07 77 07 77 81 07 77 07

Barleeia unifasciata Montagu, 1803 ----- + --- Bittium reticulatum da Costa, 1778 + ---- + --- Cingula cingillus Montagu, 1803 + ------Gibbula pennanti Philippi, 1846 - + - + -- + - + Gibbula sp. Risso, 1826 + - + ---- + - Gibbula umbilicalis da Costa, 1778 - - + + + + + - + Littorina litorea Linnaeus, 1758 - - + - + + - - - Littorina obtusata Linnaeus, 1758 + + + + + + + + + Q10: Please Littorina saxatilis Olivi, 1792 + + + + - + + - - conﬁ rm Manzonia crassa Kammacher, 1798 ----- + --- the change Melarhaphe neritoides Linnaeus, 1758 + + + + - + + - - from ‘184’ Monodonta sp. Lamarch, 1799 - - + + + + + - - to ‘1841’ in Odostomia sp. Fleming, 1813 ----- + --- Table 4 Omalogyra atomus Philippi, 1841 ----- + --- Patella depressa Pennant, 1777 + + - - + + + - - Patella pellucida Linnaeus, 1758 ----- + --- Patella sp. Linnaeus, 1758 - - + + + - + - - Patella vulgata Linnaeus, 1758 - + + + - + + + + Peringia ulvae Pennant, 1777 + ------Rissoa parva da Costa, 1778 ----- + --- Skeneopsis planorbis Fabricius O., 1780 ----- + --- Tricolia pullus Linnaeus, 1758 ----- + --- * Pelvetia canaliculata (PC), Fucus spiralis (FS), Fucus vesiculosus (FV), and Ascophyllum nodosum (AN).

Q11: Can this be changed to ‘0.25 individual m-2’? in Figure 4 Seasonal changes in gastropod species densities recorded in (A, B) Pelvetia canaliculata , (C, D) Fucus spiralis , (E, F) F. vesiculo- Figure 4 sus , and (G) Ascophyllum nodosum assemblages. caption Densities are shown as individuals 0.25 m-2 . Isolated large black circles indicate that the species was present for only several months in 1977.

in the frequency and timing of upwelling episodes will and seasonality (Llope et al. 2006 ) of summer upwelling modify nutrient availability and temperature, both main fac- along the north coast of Spain, and relate this tendency to tors determining seasonality of biomass cycle in seaweeds. global warming. Several studies show a decreasing trend in the intensity The balance between grazers and fucoids must also (Laví n et al. 2000, Cabanas et al. 2003 , Llope et al. 2006 ) be taken into account. In 2007, some littorinid species Article in press - uncorrected proof

C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain 7

were less common in the uppermost intertidal assemblage is considered responsible for recent phenological changes ( P. canaliculata) than 30 years before (e.g., Littorina in both fauna and fl ora (Hughes 2000 , Walther et al. 2002 , obtusata). Conversely, higher densities of Gibbula pennanti Parmesan and Yohe 2003 , Root et al. 2003 , Dunn 2004 , (Philippi 1846) and G. umbilicalis (da Costa 1778) occurred Visser and Both 2005 , Moore et al. 2011 ). If the observed in the lowermost intertidal zone (F. vesiculosus assem- changes are a response of fucoid species to warming and not blage); these increases are congruent with increases pre- merely interannual fl uctuations in biomass pattern, it would dicted for gastropods as a result of warming (Mieszkowska imply that these species will experience the most important et al. 2006, 2007 ). In order to evaluate the stability of the changes, which would be evident as a drastic reduction in balance between fucoid biomass and grazer density in 1977 their abundance on the north coast of Spain. Examples of this and 2007, we used a model based on prey-predator isoclines kind of changes would be the 245 km northward withdrawal (Noy -Meir 1975 , May 1977 ). Figure 4 shows that the area of of P. canaliculata along the Portuguese coast (Lima et al. stability in the system may have changed due to a shift from 2007 ); 3 years later (2010) on the shore we studied, F. vesicu- a state with high biomass of fucoids and low density of herbi- losus disappeared and the sizes of the canopies of P. canali- vores to another in which biomass and production of fucoids culata and F. spiralis were severely reduced (C. Fern á ndez, decreased, and density and grazing pressure of herbivores personal observations) have slightly increased (Hawkins et al. 2009 ). As a result, the space where the system is in stable equilibrium has been reduced, with P. canaliculata (Figure 4 A) and F. vesiculosus Acknowledgments (Figure 4 C) assemblages being most sensitive to this shift, especially F. vesiculosus . C. Lamela-Silvarrey gratefully acknowledges a grant from Obra Not all ecological changes in intertidal species distribu- Social La Caixa and a predoctoral fellowship (FPU) from the tions and abundances should be attributed to global warming. Ministry of Education and Science of Spain. We would like to thank Long-term changes in the abiotic environment can mimic the F.G. Taboada for the SST data kindly provided, Miguel Garc í a Porras for the technical support, and J.M. Rico and L. Blanco Moro for the effect of climate change (Denny and Paine 1998 ). Therefore, language correction assistance. The manuscript profi ted from the our results should only be considered as an evidence of helpful comments from anonymous reviewers. This study was sup- change, without inferring causal mechanisms, and should ported by the Ministry of Education and Science of Spain, within the be carefully evaluated by the quality of the time-series data project “ Caracterizaci ó n y modelizació n de los patrones de variació n analyzed. Nevertheless, in spite of this qualifi cation, the gen- espacial y temporal de las comunidades costeras en Asturias ” (CTM eral trend of increasing temperature due to climate change 2006-05588).

Q12: Figure 5 was not cited in text. Please Figure 5 Noy-Meir models of the balance between fucoid biomass (real data) and herbivores density (postulated data) in 1977 and 2007. supply Gray arrows represent the range in which the system is in a state of unstable equilibrium. (A) Pelvetia canaliculata , (B) Fucus spiralis , (C) citation in the F. vesiculosus , (D) and Ascophyllum nodosum . F, fucoid biomass; H, herbivores density; NPP, net primary production; DW, dry weight; text Vm , maximum biomass; Vx , biomass at which growth is maximum. Article in press - uncorrected proof

8 C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain

Q13: References Fischer-Piette, E. and J.M. Gaillard. 1959. Les patelles au long des Please confi rm cô tes atlantiques Ibé riques et Nord-Marocaines. J. Conchol. 99: the change for Airoldi, L. and M.W. Beck. 2007. Loss, status and trends for coastal 135 – 200. ref. Anad ó n, marine habitats of Europe. Oceanogr. Mar. Biol. 45: 345 – 405. Fraga, F. 1981. Upwelling off the Galician Coast, northwestern and Niell. In Coastal upwelling (1981) Anad ó n, R. 1980. Estructura y diná mica del sistema litoral rocoso Spain. : (F.A. Richards, ed.) . Vol. 1 (Coastal de las costas de Asturias. Memoria Policopiada Fundació n Juan & Estuarine Sciences Series). American Geophysical Union, Q14: March, Madrid, Spain. pp. 252. Washington, DC. pp. 176 – 182. Please confi rm Gonz á lez, G.R. and R. Anad ó n. 1981. Din á mica de Hyale nilssoni the change Anad ó n, R. and F.X. Niell. 1981. Distribució n longitudinal de mac- in author’s r ó fi tos en la costa asturiana (N. de Espa ñ a). Invest. Pesq. 45: (Rathke) (Amphipoda, Talitridae) en el horizonte de Pelvetia canaliculata de Ba ñ ugues (Asturias). Oecol. Aquat. 5: 207 – 218. name for refs. 143 – 156. Q19: Appeltans An á lisis de esce- Anad ó n, R. and C. Fern á ndez. 1984. Algunas consideraciones sobre Gonz á lez-Taboada, F. and R. Anad ó n-Alvarez. 2011. Please supply et al. (2010) la estimació n de la producció n primaria en horizontes intermar- narios de cambio climá tico en Asturias. Gobierno del Principado and Arrontes complete eales. Cuad. Á rea Cienc. Mar. Sem. Est. Galegos 1: 183 – 187. de Asturias, Consejerí a de Medio Ambiente, Ordenació n del Junquera date when (1983) Appeltans, W., P. Bouchet, G.A. Boxshall, K. Fauchald, D.P.H. Territorio e Infraestructuras, Oviedo, Spain. pp. 128. the site was Gordon, B.W. Hoeksema, G.C.B. Poore, R.W.M. van Soest, Guiry, M.D. and G.M. Guiry. 2010. AlgaeBase. World-wide elec- accessed for Q15: Please S. St ö hr, T.C. Walter and M.J. Costello. 2010. World Register tronic publication, National University of Ireland, Galway ref. Guiry supply of Marine Species (WoRMS), http://www.marinespecies.org. (Ireland), http://www.algaebase.org. Accessed XX June, 2010. and Guiry complete date when the site Accessed XX June, 2010. Hawkins, S.J. and R.G. Hartnoll. 1983. Grazing of intertidal algae by (2010) was accessed Ardr é , F. 1970. Contribution a l ’ é tude des algues marines du Portugal. marine invertebrates. Oceanogr. Mar. Biol. 21: 195 – 282. for ref. I. La Flore. Port. Acta Biol. Ser. B 10: 1 – 415. Hawkins, S.J. and R.G. Hartnoll. 1985. Factors determining the upper Appeltans et al. Ardr é , F. 1971. Contribution à l ’ é tude des algues marines du Portugal. limits of intertidal canopy-forming algae. Mar. Ecol.: Prog. Ser. (2010) II. Ecologie et Chorologie. Bull. Cent. Etud. Rech. Sci., Biarritz 20: 265 – 271. Q16: 8: 359 – 374. Hawkins, S.J., R.G. Hartnoll, J.M. Kain and T.A. Norton. 1992. Plant- Please confi rm Arrontes Junquera, J. 1983. Estudio ecoló gico del horizonte de animal interactions on hard substrata in the north-east Atlantic. the change in Fucus vesiculosus . Biolog í a de Dynamene bidentata . Ph.D. In: (D.M. John, S.J. Hawkins and J.H. Price, eds.) Plant-animal author’s name. Please note Dissertation, Universidad de Oviedo, Oviedo, Spain. pp. 93. interactions in the marine benthos . Clarendon Press, Oxford, occurrences Arrontes Junquera, J.M. 1987. Estrategias adaptativas de isó podos UK. pp. 1 – 33. of J. Arrontes, en la zona intermareal. Ph.D. Thesis, Universidad de Oviedo, Hawkins, S.J., P.J. Moore, M.T. Burrows, E. Poloczanska, N. J. Arrontes Oviedo, Spain. pp. 501. Mieszkowska, R.J.H. Herbert, S.R. Jenkins, R.C. Thompson, Q20: Junquera, and Arrontes, J. 1990. Composition, distribution on host, and seasonality M.J. Genner and A.J. Southward. 2008. Complex interactions in Please J.M. Arrontes of epiphytes on three intertidal algae. Bot. Mar. 33: 205 – 211. a rapidly changing world: responses of rocky shore communities confi rm the Junquera in change in this list Ballantine, W.J. 1961. A biologically defi ned exposure scale for the to recent climate change. Clim. Res. 127: 123 – 133. comparative description of rocky shores. Field Studies 1: 1 – 19. Hawkins, S.J., H.E. Sudgen, N. Mieszkowska, P.J. Moore, E. author’s name Botas, J.A., E. Fern á ndez, A. Bode and R. Anad ó n. 1990. A persis- Poloczanska, R. Leaper, R. Herbert, M.J. Genner, P.S. Moschella, for refs. Q17: tent upwelling off the Central Cantabrian Coast (Bay of Biscay). R.C. Thompson, S.R. Jenkins, A.J. Southward and M.T. Burrows. Hawkins et Please confi rm Estuar. Coast. Shelf Sci. 30 2009. Consequences of climate-driven biodiversity changes for : 185 – 199. al. (2009) additional Cabanas, J.M., A. Lav í n, M.J. Garc í a, C. Gonz á lez-Pola and E.T. ecosystem functioning of north European rocky shores. Mar. information and Lima et Ecol.: Prog. Ser. 396: 245 – 259. for refs. Botas Pé rez. 2003. Oceanographic variability in the northern shelf al. (2007) et al. (1990), of the Iberian Peninsula (southern Bay of Biscay). 1990 – 1999. Helmuth, B., N. Mieszkowska, P. Moore and S. Hawkins. 2006. Cabanas et ICES Mar. Sci. Symp. 219: 71 – 79. Living on the edge of two changing worlds. Forecasting the al. (2003) Chapman, A.R.O. 1995. Functional ecology of fucoid algae: twenty- responses of rocky intertidal ecosystems to climate change. Dunn (2004), three years of progress. Phycologia 34: 1 – 32. Annu. Rev. Ecol. Evol. Syst. 37: 373 – 404. Fraga (1981), Denny, M.D. and R.T. Paine. 1998. Celestial mechanics, sea-level Hughes, L. 2000. Biological consequences of global warming: is the Gonzá lez- Taboada, changes, and intertidal ecology. Biol. Bull. 194: 108 – 115. signal already apparent ? Trends Ecol. Evol. 15: 56 – 61. and Anad ó n- Dunn, P. 2004. Breeding dates and reproductive performance. In : Knight, M. and M.W. Parke. 1950. A biological study of Fucus Alvarez (2011), (A.P. M ø ller, W. Fiedler, P. Berthold and H. Caswell, eds.) Birds vesiculosus and Fucus serratus . J. Mar. Biol. Assoc. U.K. 29: Lima et al. and climate change. Vol. 35 (Advances in Ecological Research 439 – 514. (2006), Llope Series). Academic Press, Amsterdam. pp. 69 – 87. Lav í n, A., G. D í az del R í o, G. Casas and J.M. Cabanas. 2000. et al. (2006), Fern á ndez, C. 2011. The retreat of large brown seaweeds on the Afl oramiento en el nororeste de la Pen í nsula Ib é rica. Í ndices de Mieszkowska ° ° et al. (2007), north coast of Spain: the case of Saccorhiza polyschides . Eur. J. afl oramiento para el punto 43 N, 11 O. Per í odo 1990 – 1999. Dat. Schonbeck and Phycol. 46: 352 – 360. Res ú m. Inst. Esp. Oceanogr. 15: 1 – 25. Norton (1978) Fern á ndez, C. and F.X. Niell. 1982. Zonaci ó n del fi tobentos inter- Lewis, J.R. 1964. The ecology of rocky shores . The English and Westlake mareal de la regió n de Cabo Peñ as (Asturias). Invest. Pesq. 46: Universities Press, London, UK. pp. 323. (1969) 121 – 141. Lima, F.P., N. Queiroz, S.J. Hawkins, P.A. Ribeiro and A.M. Santos. Fischer-Piette, E. 1955. R é partition le long des c ô tes septentrionales 2006. Recent changes in the distribution of a marine gastropod, Q18: de l ’ Ë spagne des principales é sp è ces peuplant les rochers inter- Patella rustica Linnaeus, 1758, and their relationships to unusual Please cotidaux. Ann. Inst. Oceonogr. (Paris) 31: 37 – 124. climatic events. J. Biogeogr. 33: 812 – 822. confi rm the Fischer-Piette, E. 1957. Sur les progr è s des esp è ces septentrionales Lima, F.P., P.A. Ribeiro, N. Queiroz, S.J. Hawkins and A.M. Santos. change for dans le bios intercotidal ib é rique: situation en 1956 – 1957. C. R. 2007. Do distributional shifts of northern and southern species refs. Fischer- Acad. Sci. 245: 373 – 375. of algae match the warming pattern? Glob. Change Biol. 13: Piette (1959) Fischer-Piette, E. 1959. Pelvetia canaliculata examin é e de proche 2592 – 2604. and Hawkins en proche de la Manche au Portugal. In : Ecologie des algues Little, C. and J.A. Kitching. 1996. The biology of rocky shores . et al. (1992) marines , Dinard (France) 20 – 28 September 1957. pp. 65 – 73. Oxford University Press, Oxford, UK. pp. 240. Article in press - uncorrected proof

C. Lamela-Silvarrey et al.: Fucoid assemblages in northern Spain 9

Llope, M., R. Anad ó n, L. Viesca, M. Quevedo, R. Gonz á lez-Quir ó s Santos, F., M. G ó mez-Gesteira1, M. deCastro and I. Á lvarez. 2011. and N.C. Stenseth. 2006. Hydrographic dynamics in the south- Upwelling along the western coast of the Iberian Peninsula: depen- ern Bay of Biscay shelf-break region: integrating the multiscale dence of trends on fi tting strategy. Clim. Res. 48: 213 – 218. physical variability over the period 1993– 2003. J. Geophys. Res. Schonbeck, M.W. and T.A. Norton. 1978. Factors controlling the 111: C09021. upper limits of fucoid algae on the shore. J. Exp. Mar. Biol. Ecol. L ü ning, K. 1990. Seaweeds: their environment, biogeography and 31: 303 – 313. ecophysiology . Wiley Interscience, New York. pp. 527. Schonbeck, M.W. and T.A. Norton. 1979. Drought-hardening in the May, R.M. 1977. Thresholds and breakpoints in ecosystems with a upper-shore seaweeds Fucus spiralis and Pelvetia canaliculata . multiplicity of stable states. Nature 269: 471 – 477. J. Ecol. 67: 687 – 696. Mieszkowska, N., M.A. Kendall, S.J. Hawkins, R. Leaper, P. Southward, A.J., S.J. Hawkins and M.T. Burrows. 1995. Seventy Williamson, N.J. Hardman-Mountford and A.J. Southward. years ’ observations of changes in distribution and abundance 2006. Changes in the range of some common rocky shore spe- of zooplankton and intertidal organisms in the western English Q21: cies in Britain – a response to climate change ? Hydrobiologia Channel in relation to rising sea temperature. J. Therm. Biol. 20: Please 555: 241 – 251. 127 – 155. confi rm Mieszkowska, N., S.J. Hawkins, M.T. Burrows and M.A. Kendall. Southward, A.J., O. Langmead, N.J. Hardman-Mountford, J. Aiken, additional information 2007. Long-term changes in the geographic distribution and G.T. Boalch, P.R. Dando, M.J. Genner, I. Joint, M.A. Kendall, N.C. (R.P. and population structures of some near-limit populations of Osilinus Halliday, R.P. Harris, R. Leaper, N. Mieszkowska, R.D. Pingree, Smith) lineatus (Gastropoda: Trochidae) in Britain and Ireland. J. Mar. A.J. Richardson, D.W. Sims, T. Smith, A.W. Walne and S.J. for ref. Biol. Assoc. U.K. 87: 537 – 545. Hawkins. 2005. Long-term oceaonographic and ecological research Southward et Moore, P.J., R.C. Thompson and S.J. Hawkins. 2011. Phenological in the western English Channel. Adv. Mar. Biol. 47: 1 – 105. al. (2005) changes in intertidal con-specifi c gastropods in response to cli- Steneck, R.S., M.H. Graham, B.J. Bourque, D. Corbett, J.M. mate warming. Glob. Change Biol. 17: 709 – 719. Erlandson, J.A. Estes and M.J. Tegner. 2002. Kelp forest eco- Q22: Noy-Meir, I. 1975. Stability of grazing systems: an application of systems: biodiversity, stability, resilience and future. Environ. Please confi rm predator-prey graphs. J. Ecol. 63: 459 – 481. Conserv. 29: 436 – 459. the change Parmesan, C. and G. Yohe. 2003. A globally coherent fi ngerprint Subrahmanyan, R. 1960. Ecological studies on the Fucales I. Pelvetia for ref. of climate change impacts across natural systems. Nature 421: canaliculata . Dcne. et Thur. J. Indian Bot. Soc. 39: 614 – 630. Subrahmanyan 37 – 42. Subrahmanyan, R. 1961. Ecological studies on the Fucales II. Fucus (1960), Visser and Both P é rez, F.F., X.A. Pad í n, Y. Pazos, M. Gilcoto, M. Cabanas, P.C. Pardo, spiralis L. J. Indian Bot. Soc. 40: 335 – 354. (2005) M.D. Doval and L. Farina-Bustos. 2010. Plankton response to Thompson, R.C., T.P. Crowe and S.J. Hawkins. 2002. Rocky inter- weakening of the Iberian coastal upwelling. Glob. Change Biol. tidal communities: past environmental changes, present status 16: 1258 – 1267. and predictions for the next 25 years. Environ. Conserv. 29: Q23: Reynolds, R.W., T.M. Smith, C. Liu, D.B. Chelton, K.S. Casey and 168 – 191. Thompson M.G. Schlax. 2007. Daily high-resolution-blended analyses for Thompson, R.C., T.A. Norton and S.J. Hawkins. 2004. Physical et al. (2004) sea surface temperature. J. Clim. 20: 5473 – 5496. stress and biological control regulate producer-consumer balance is missing Root, T.L., J.T. Price, K.R. Hall, S.H. Schneider, C. Rosenzweig and in intertidal biofi lms. Ecology 85: 1372 – 1382. from the list J.A. Pounds. 2003. Fingerprints of global warming on wild ani- Visser, M.E. and C. Both. 2005. Shifts in phenology due to global of references. mals and plants. Nature 421: 57 – 60. climate change: the need for a yardstick. Proc. Biol. Sci. 272: Please supply Ruiz Villareal, M., X.A. Á lvarez Salgado, J.M. Cabanas, F. Fern á ndez 2561 – 2569. citation or P é rez, C. Gonz á lez Castro, J.L. Herrera Cortijo, S. Piedracoba Walther, G.R., E. Post, P. Convey, A. Menzel, C. Parmesan, T.J.C. delete from Varela and G. Ros ó n Porto. 2009. Variabilidade clim á tica e ten- Beebee, J.M. Fromentin, O. Hoegh-Guldberg and F. Bairlein. list dencias decadais nos forzamentos metereol ó xicos e as propie- 2002. Ecological responses to recent climate change. Nature 416: dades das uagas adxacentes a Galicia. In : (Conseller í a de 389 – 395. Medio Ambiente e Desenvolvemento Sostible, ed.) Evidencias Westlake, D.F. 1969. Macrophytes. In : (R.A. Vollenweider, J.F. e Impactos do Cambio Climá tico en Galicia. Xunta de Galicia, Talling and D.F. Westlake, eds.) A manual on methods for Santiago de Compostela, Spain. pp. 271 – 286. measuring primary production in aquatic environments , IBP Sagarin, R.D., J.P. Barry, S.E. Gilman and C.H. Baxter. 1999. Climate Handbook, no. 12. Blackwell, Oxford. pp. 25 – 32. related change in an intertidal community over short and long time scales. Ecol. Monogr. 69: 465 – 490. Received 24 November, 2011; accepted 30 January, 2012