Increasing sea surface temperature and range shifts of intertidal gastropods along the Iberian Peninsula

Journal of Sea Research 77 (2013) 1–10

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Increasing sea surface temperature and range shifts of intertidal gastropods along the Iberian Peninsula Marcos Rubal a, b,⁎, Puri Veiga a, b, Eva Cacabelos c, Juan Moreira d, Isabel Sousa-Pinto a, b a

Laboratory of Coastal Biodiversity, Centre of Marine and Environmental Research (CIIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s/n 4150-181 Porto, Portugal Centro Tecnológico del Mar-Fundación CETMAR, C/Eduardo Cabello s/n, 36208, Vigo, Spain d Departamento de Biología (Zoología), Universidad Autónoma de Madrid, Cantoblanco, E-28049 Madrid, Spain b c

a r t i c l e

i n f o

Article history: Received 10 July 2012 Received in revised form 5 December 2012 Accepted 8 December 2012 Available online 31 December 2012 Keywords: Climate Change Sea Temperature Intertidal Gastropods Range Boundaries Iberian Peninsula North-eastern Atlantic

a b s t r a c t There are well-documented changes in abundance and geographical range of intertidal invertebrates related to climate change at north Europe. However, the effect of sea surface warming on intertidal invertebrates has been poorly studied at lower latitudes. Here we analyze potential changes in the abundance patterns and distribution range of rocky intertidal gastropods related to climate change along the Iberian Peninsula. To achieve this aim, the spatial distribution and range of sub-tropical, warm- and cold-water species of intertidal gastropods was explored by a fully hierarchical sampling design considering four different spatial scales, i.e. from region (100 s of km apart) to quadrats (ms apart). Variability on their patterns of abundance was explored by analysis of variance, changes on their distribution ranges were detected by comparing with previous records and their relationship with sea water temperature was explored by rank correlation analyses. Mean values of sea surface temperature along the Iberian coast, between 1949 and 2010, were obtained from in situ data compiled for three different grid squares: south Portugal, north Portugal, and Galicia. Lusitanian species did not show significant correlation with sea water temperature or changes on their distributional range or abundance, along the temperature gradient considered. The sub-tropical species Siphonaria pectinata has, however, increased its distribution range while boreal cold-water species showed the opposite pattern. The latter was more evident for Littorina littorea that was almost absent from the studied rocky shores of the Iberian Peninsula. Sub-tropical and boreal species showed significant but opposite correlation with sea water temperature. We hypothesized that the energetic cost of frequent exposures to sub-lethal temperatures might be responsible for these shifts. Therefore, intertidal gastropods at the Atlantic Iberian Peninsula coast are responding to the effect of global warming as it is happening at higher latitudes. However, the identity of the species showing changes in their range of distribution was different. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Climate change is widely recognized as a major threat to global biodiversity and this is expected to intensify over time (IPCC, 2007). This environmental warming is also reflected in the considerable increase in sea surface temperature (SST) during the last decades (e.g. Burrows et al., 2011; Lima and Wethey, 2012). However, this trend is far from being uniformly distributed along the oceans and the Atlantic Ocean shows one of the largest increases, suffering the most rapid environmental and biological changes (Hawkins et al., 2008; Lima and Wethey, 2012). Climatic and oceanographic conditions control a wide

⁎ Corresponding author at: Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s/n 4150-181 Porto, Portugal. Tel.: +351 223401800; fax: +351 223390608. E-mail address: [email protected] (M. Rubal). 1385-1101/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.seares.2012.12.003

number of biological and ecological processes such as species ranges, biological interactions, reproductive output, metabolism or larval dispersal (Allen et al., 2002; O'Connor et al., 2006; Southward et al., 1995; Veiga et al., 2011). Therefore, SST rising may affect marine biota in different ways and at different scales (Brierley and Kingsford, 2009). For example, there have been documented shifts in the geographic range of species distribution and changes in biotic interactions and composition of planktonic, pelagic, demersal and benthic assemblages (e.g. Davis et al., 1998; Edwards and Richardson, 2004; Hawkins et al., 2008). Early biogeographic studies correlated species distribution with temperature and still form the basis of ecological principles today (Helmuth et al., 2006). Therefore, changes in abundance and shifts in the distributional boundaries have frequently been linked to changes in seawater and air temperatures (Espinosa et al., 2010). Many studies have proved that temperature plays a central role shaping the distribution and abundance patterns of intertidal invertebrates (Mieszkowska et al., 2006, 2007). Intertidal organisms have proved to be good models for the study of the dynamic and processes at the range boundaries,

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M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

because they are easy to manipulate and have almost linear geographic distribution (Sagarin and Gaines, 2002). Moreover, they live in the interface of land and sea and thus are subjected to the environmental conditions and changes of aquatic and aerial climatic regimens, frequently living in the limit of their physiological tolerances (Helmuth et al., 2006). These effects are difficult to determine experimentally so monitoring studies have been shown to be very useful for this task (e.g. Edwards and Richardson, 2004; Helmuth et al., 2006; Southward et al., 1995). During the last decades, changes in the abundance and shifts in geographical range of intertidal organisms on the coast of U.K. have been recorded and related to climate changes (Southward et al., 1995; Mieszkowska et al., 2006, 2007; Wethey et al., 2011). However, most of the studies on this issue at NE Atlantic have been made in the U.K., where Lusitanian warm-water species (WWS) reach their northern boundary. On the other hand, at lower latitudes (i.e. Iberian Peninsula coast) where boreal cold-water species (CWS) reach their southern boundary, studies are scarce (Lima et al., 2006) or old (Fischer-Piétte, 1960, 1963). This lack of data from lower latitudes can potentially skew future predictions about the effects of global warming and, so, an increase on the research effort on the southern boundary of CWS is needed. Similarly to Ireland and Britain, the coast of the Iberian Peninsula is a boundary region where warm- and cold-water intertidal species reach their northern or southern geographic distribution limit (Ardré, 1971; Pereira et al., 2006). In the North of Spain, the warmer water of the Cantabrian Sea (southernmost part of the Bay of Biscay) favors the abundance of WWS and sub-tropical species from the Basque province to Asturias; on the contrary, many CWS are found on the Galician coast following this Cantabrian gap in their distribution (Fischer-Piétte, 1956; Southward et al., 1995). This limit is, however, highly variable and environmental changes have modified it significantly along last century (Fischer-Piétte, 1955, 1956, 1958) and also recently (Fernández, 2011). On the other hand, the cold water input due to the upwelling during the spring and summer months, allows CWS to eventually reappear in the Galician coast and to some extent to the Portuguese coast where they reach their southern limit of distribution (e.g. Ardré, 1971; Lima et al., 2007; Pereira et al., 2006). Intertidal gastropods play a central role in shaping intertidal assemblages (Coleman et al., 2006; Underwood, 1980); some species are conspicuous, relatively large sized, easy to count and measure and therefore suitable to evaluate their population features and distribution. Some studies have shown changes in their distribution, abundance and phenology due to the effect of the global warming (Mieszkowska et al., 2006, 2007; Moore et al., 2011). Therefore, intertidal gastropods could be used as valuable indicators of the effects of global warming in intertidal assemblages. Many species of intertidal gastropods show in the Iberian Peninsula either their southern limit of distribution (e.g. the limpet, Patella vulgata Linnaeus, 1758; the dog whelk, Nucella lapillus (Linnaeus, 1767); the periwinkles, Littorina saxatilis (Olivi, 1792) and Littorina littorea (Linnaeus, 1758)) or their northern limit (e.g. the sub-tropical pulmonate false limpet, Siphonaria pectinata (Linnaeus, 1758)). Moreover, the abundance of WWS could be driven by the important SST gradient along the Iberian Peninsula coast. Historical records on the abundance and distribution range of intertidal gastropods at the Atlantic Iberian Peninsula are not as extensive as those from Ireland and British coasts but there are some valuable data from the XX century (Fischer-Piétte, 1956; Hidalgo, 1917; Nobre, 1940). Anyway, few studies have focused their attention on the potential changes in distribution and abundance of intertidal gastropods at the Atlantic Iberian Peninsula and their possible relationship to global warming (but see Lima et al., 2006). The aim of this study is to explore changes on the spatial pattern of abundance and on the distribution range of intertidal gastropod species along the SST gradient of the Atlantic coast of the Iberian Peninsula. Moreover, the potential relationship between the abundance of the selected species and the SST will be explored.

2. Material and methods 2.1. Study area The study area encompassed approximately 885 km between latitudes (37° 31′ 22.45″ N) and (43° 40′ 37.55″ N); from Galician (NW Spain) to Portuguese continental coasts, with the exception of the southernmost coast of Portugal (i.e. Algarve). The coast was divided in five regions: A Mariña (AM), Costa da Morte (CM), North Portugal (NP), Central Portugal (CP) and South Portugal (SP) corresponding to the main stretches of rocky coastline (Fig. 1). This area presents a semidiurnal tidal regime, with the largest spring tides of 3.5–4.0 m. The wave regime is dominated by swells from the NW (73%) with those from the W contributing 16%. The mean wave height varies strongly among seasons. In the spring-summer period, typical wave heights are between 1 and 3 m. Most storms occur during autumn–winter months (October–March) when wave heights often exceed 7 m (Dias et al., 2002). The whole study area is affected by seasonal upwelling events; these processes differ, however, among the five considered regions. In AM upwelling events are restricted from July to August and affect only the shelf (Ospina-Álvarez et al., 2010). Costa da Morte presents longer upwelling events (from April to September) than those of AM; the upwelling events there affect mainly the shelf but they can also affect other nearby coastal regions (Prego and Bao, 1997). Upwelling events in the three regions studied in Portugal (NP, CP and SP) present the same seasonal periodicity as CM (from April to September) but the upwelling affects also the coastal regions (Ospina-Álvarez et al., 2010). The surface phytoplankton pigment concentration shows a general decrease from North to South and an important seasonal variability related to upwelling, inland inputs and oceanic circulation (Peliz and Fiúza, 1999). Sea surface temperature (SST) shows a latitudinal gradient from AM to SP and significant seasonal changes with a maximum latitudinal variation of 8 °C in autumn and a minimum of 4 °C in winter (Gómez-Gesteira et al., 2008). The morphology and geological composition of the shore is also variable among the studied regions. Thus, rocky shores at AM and CM show a significant slope and correspond mainly to granitic rocks; rocky shores at NP show a gentle slope and are mostly composed by a mixture of granite greywacke and schist. Finally, rocky shores at CP and SP are mainly flat platforms made up of sandstone. 2.2. Temperature trends Mean values of SST along the Atlantic Iberian coast, between January 1949 and December 2010, were obtained from in situ raw data compiled by the International Comprehensive Ocean–Atmosphere Data Set (ICOADS; Woodruff et al., 1988). Data for three different grid squares: south Portugal (37–38° N, 09–10° W), north Portugal (41-42° N, 09-10° W), and Galicia (43–44° N, 09–10° W) were selected. To avoid bias due to different daytime measurements, only data from 12:00 h were used. The mean values of those years with low number of date or data restricted only to one season were not considered. 2.3. Target species and sampling A set of WWS, CWS and sub-tropical intertidal gastropods, based on Southward et al. (1995), was defined before sampling and determined as target species. The following species were considered as representative of CWS: P. vulgata, L. saxatilis, L. littorea and N. lapillus. The set of WWS was composed by the top shells, Gibbula umbilicalis (da Costa, 1778) and Osilinus lineatus (da Costa, 1778), the black periwinkle, Melarhaphe neritoides (Linnaeus, 1758), the limpet, Patella depressa Pennant, 1777, and as sub-tropical species S. pectinata. Sampling was done during the spring tides of July and August 2011. A fully hierarchical sampling design was used to study the spatial distribution of the target gastropods. The first spatial scale of sampling

M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

3

N

AM

44oN Bu

Ll Rn

Ml Ba Mu

43oN

42oN

Oi Mo

NP

Vi

41oN

Ag

40oN

39oN

Pe

CP

Ri Ma

38oN

SP

Ol Al

Zm

o

37 N 11oW

10oW

9oW

8oW

7oW

Fig. 1. Location of the 16 studied shores along the Atlantic coast of the Iberian Peninsula. Region and Shore codes are explained in Table 1. Note that due to the lack of S. pectinata at Oia (NP) this species was sampled instead at Aguda to maintain a balanced design.

corresponds to that of the five aforementioned regions (i.e. AM, CM, NP, CP, SP) separated from each other by 100s of km. Within each region, three rocky shores, separated by 10s of km, were selected (Fig. 1; Table 1). Within each of these shores, three sites, separated by 10s of ms, were randomly selected. At each site, five quadrats (50×50 cm) were sampled at midshore (2–2.5 m above low tide; height varied slightly among shores) where the target species are typically present. All the gastropods within each quadrat were identified and quantified in situ. Because of the small size of the individuals, numbers of M. neritoides were determined by sampling three quadrats (10 × 0 cm) at each site at high-shore; all individuals within any quadrat were collected and preserved in 70% ethanol and then sorted and counted at the laboratory. 2.4. Data analyses In order to explore the geographic distribution and compare the relative abundance of the target species among the selected shores, the mean values of each species was represented graphically from the southern to the northern shores. Expansion or retractions on the range of distribution of the species over time were calculated as the difference in Km between the northern or southern limit found in our study and previous limits recorded by other authors; mainly Hidalgo (1917) and Nobre (1940). The spatial abundance patterns of the studied taxa were examined by means of a 3-way nested analysis of variance (ANOVA). Data were analyzed using a balanced fully-nested design with three random factors: region (5 levels), shore (3 levels, nested in region) and site (3 levels, nested in location and region) (n=5); the design for S. pectinata, N. lapillus and L. saxatilis was similar as the described above but the factor region presented 3 levels instead of 5 due to their restricted distribution range. Finally, for M. neritoides analyses, as explained above, three replicates were used instead of five. Prior to the analysis, the Cochran's C-test was employed to assess homogeneity of variances. If

necessary, data were transformed to achieve homogeneity. If homogeneity was not achieved after transformation, untransformed data were analyzed and the more stringent criterion of P b 0.01 was used to reject null hypotheses (Underwood, 1997). Mean squares (MS) estimates were used to assess the variation associated with each studied spatial scale. This was done by dividing the difference between the MS of the term of interest and that of the term hierarchically below by the product of the levels of all terms below that of interest. Negative estimates of variance were removed from the analysis and all other values recalculated following the procedure described by Fletcher and Underwood (2002). Estimates of spatial variation were reported as percentages of actual variances to establish the magnitude of each scale contribution to patterns of distribution. Analyses for the calculation of variance components were done on untransformed data to provide variance components comparable Table 1 Location of the studied shores along the Iberian Peninsula. Region

Shore

Latitude

A Mariña (AM)

Rinlo (Rn) Llas (Ll) Burela (Bu) Barrañán (Ba) Malpica (Ml) Muxía (Mu) Oia (Oi) Moledo (Mo) Viana (Vi) Aguda (Ag)⁎

43° 33′ 38.76″ 43° 34′ 50.86″ 43° 40′ 37.55″ 43° 18′ 45.48″ 43° 19′ 28.35″ 43° 05′ 59.71″ 42° 00′ 10.88″ 41° 50′ 29.53″ 41° 41′ 49.79″ 41° 02′ 43.22″ 39° 22′ 13.57″ 38° 59′ 15.44″ 38° 51′ 00.47″ 37° 53′ 27.33″ 37° 39′ 12.14″ 37° 31′ 22.45″

Costa da Morte (CM) North Portugal (NP)

Central Portugal (CP) South Portugal (SP)

Peniche (Pe) Ribeira de Ilhas (Ri) Magoito (Ma) Oliveirinha (Ol) Almograve (Al) Zambujeira do Mar (Zm)

⁎ At Aguda only Siphonaria pectinata was sampled.

Longitude N N N N N N N N N N N N N N N N

7° 7° 7° 8° 8° 9° 8° 8° 8° 8° 9° 9° 9° 8° 8° 8°

6′ 36.80″ W 15′ 56.70″ W 22′ 49.33″ W 33′ 41.07″ W 48′ 40.74″ W 13´ 16.11″ W 52′ 45.57″ W 52′ 28.67″ W 51′ 10.52″ W 39′ 10.31″ W 23′ 14.59″ W 25′ 7.00″ W 27′ 20.10″ W 47′ 47.47″ W 48′ 5.77″ W 47′ 12.59″ W

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across all data. All the univariate analyses were done using the GMAV5 programme (University of Sydney, Australia). Finally, in order to explore the relationship between the abundance of target species and SST, rank correlation analyses were done for each of the species. Due to the non-normal distribution of the data we selected the Spearman's rank correlation. For each locality we considered the average SST from 60 days before the sampling date. Daily SST data for each shore were obtained from the open access repository of Meteogalicia (http://www.meteogalicia.es/observacion/satelite/). 3. Results 3.1. Temperature trends The mean annual SST from 1949 to 2010 showed a latitudinal gradient with higher values at the southern points and lower values at the north of Portugal and Galicia (Fig. 2). The information provided by Fig. 2 should be interpreted with caution (especially values for single years) due to the lack of SST data for some years and the changeable number of data among years and between seasons within each year. However, an increasing trend of mean SST was found for the three regions. 3.2. Spatial distribution 3.2.1. Melarhaphe neritoides This species was present at all shores showing the highest abundance at Viana (Fig. 3). Abundance showed significant variability at the scales of shore and site (Table 2). Percentages of actual variance showed that most variability occurred at the scale of shore. Next important components of variation were the scales of site and the residual, which indicates variance among quadrats. Variability among regions was negligible (Fig. 4). 3.2.2. Littorina saxatilis This species was restricted to the northern regions (all shores at AM -apart from Rinlo-, CM, NP; Fig. 3) retracting its range of distribution about 400 km northern than previous records by Hidalgo (1917) and Nobre (1940). Abundance showed significant variability among shores and sites (Table 2). The percentages of actual variance indicated that most variability occurred at the smallest spatial scale (among quadrats) and variability decreased when the considered spatial scale increased (Fig. 4).

South Portugal North Portugal Galicia

20

Mean annual SST (oC)

19 18 17 16 15 14 13 1940

1950

1960

1970

1980

1990

2000

2010

Fig. 2. Mean annual sea surface temperature (SST) for 1949–2010 of south Portugal (grid square 37–38° N, 09–10° W), north Portugal (grid square 41–42° N, 09–10° W) and Galicia (grid square 43–44° N, 09–10° W).

3.2.3. Littorina littorea This species was absent at the sampled tidal level at all shores. We could only find few individuals living among fucoid macroalgae at Viana. Due to the lack of data no analyses could be done.

3.2.4. Patella depressa This limpet was found at all shores in high numbers (15–60 individuals per 0.25 m 2). Abundance did not show significant variability among regions (Table 2) but increased from south to north (Fig. 3); significant differences were detected among shores and sites. The percentages of actual variance for this species indicated that most variability occurred at the smallest spatial scale (quadrats) and variability decreased when the considered spatial scale increased (Fig. 4). 3.2.5. Patella vulgata This species was present at all shores although abundance tended to increase from south to north, reaching its highest values at CM (Fig. 3). Abundance only showed significant variability at the scale of shore (Table 2). The percentages of actual variance indicated that most variability occurred at the scale of shore followed by those of quadrat and region. Variability at the scale of site was negligible (Fig. 4).

3.2.6. Gibbula umbilicalis This species was found at all shores being relatively abundant in most of them (>5 individuals per 0.25 m2 in 11 out of 15 shores, Fig. 3). Abundance showed significant variability at the scale of shore and site (Table 2). The percentages of actual variance showed that most variability for this species occurred at the scale of quadrat. Next important components of variation were the scales of shore and site. Variability among regions was negligible (Fig. 4). 3.2.7. Osilinus lineatus This species was present at all shores except for Magoito and Peniche and was particularly abundant at Viana (Fig. 3). Abundance showed significant variability among shores and sites (Table 2). The percentages of actual variance showed that most variability for this species occurred at the scale of shore. Next important components of variation were the residual, site and region (Fig. 4).

3.2.8. Nucella lapillus This species was present at all northern shores (AM -except Rinlo-, CM, NP) but it was not found at CP and SP (Fig. 3) retracting its range of distribution about 400 km northern than previous records by Hidalgo (1917) and Nobre (1940). Abundance (where present) did not show significant variability at any of the studied spatial scales (Table 2). The percentages of actual variance showed that most variability occurred at the scale of quadrat. Next important components of variation were the scales of region and site. Variability among shores was negligible (Fig. 4). 3.2.9. Siphonaria pectinata This species was present at all shores in Portugal (NP, CP, and SP) but it was not found at CM and AM (Fig. 3) expanding its range of distribution about 185 km northern than previous records by Hidalgo (1917) and Nobre (1940). Abundance seemed to decrease from south to north, reaching its maximum value at the southernmost regions (MP, SP). Abundance (where present) did not show significant variability among regions or shores (Table 2). There were significant differences among sites instead. The percentages of actual variance indicated that most variability occurred at the smallest spatial scale and variability decreased when the considered spatial scale increased, with the exception of region, that showed higher variability than that found for the scale of shore (Fig. 4).

M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

25

Melarhaphe neritoides

Littorina saxatilis

Abundance (N 0.25 m -2)

Abundance (N 0.01 m -2)

400

300

200

100

20 15 10 5 0

0

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn 16

Patella depressa

Abundance (N 0.25 m -2)

Abundance (N 0.25 m -2)

80

60

40

20

12 10 8 6 4 2

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn

Abundance (N 0.25 m -2)

Abundance (N 0.25 m -2)

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn 25

Gibbula umbilicalis

20 15 10 5

20 15 10 5

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn 20

Nucella lapillus

Abundance (N 0.25 m -2)

Abundance (N 0.25 m -2)

Osilinus lineatus

0

0

5

Patella vulgata

14

0

0

25

5

4 3 2 1 0

18

Siphonaria pectinata

16 14

SP CP NP CM AM

12 10 8 6 4 2 0

Zm Al Ol Ma Ri Pe Vi Mo Oi Mu Ml Ba Bu Ll Rn

Zm Al Ol Ma Ri Pe Ag Vi MoMu Ml Ba Bu Ll Rn

Fig. 3. Abundance of target species (Mean number (N) of individuals + SE; n = 15 quadrats) at each studied shore. AM, A Mariña; CM, Costa da Morte; NP, North Portugal; CP, Central Portugal; SP, South Portugal.

3.3. Relationship between abundance of gastropods and SST

4. Discussion

Rank correlation analyses showed that CWS have a significant negative relationship with SST (Fig. 5). The relationship between the abundance of L. littorea and SST could not be studied due to the lack of this species at the studied shores. On the other hand, the sub-tropical S. pectinata showed a significant positive relationship with SST (Fig. 5). In contrast, all the WWS showed no significant relationship with SST (Fig. 5).

Despite the limitations of the SST data set previously mentioned, SST at the Atlantic coast of the Iberian Peninsula showed a general increase along the last 60 years. This trend was also found by other authors (e.g. Gómez-Gesteira et al., 2008). However, the effect of this increase on intertidal organisms is still poorly studied at the Iberian Peninsula. Our results showed that the most abundant and common gastropods were WWS such as M. neritoides, P. depressa, G. umbilicalis and

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M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

Table 2 Results of ANOVAs testing for spatial differences in the abundance of the target species at the scales of region, shore and site. Significant values in bold; ns, not significant (P >0.05). Region Df

Shore MS

F

Melarhaphe neritoides 4 5.881 0.55 Transformation Ln(x) Cochran's C-test = 0.0965 Littorina saxatilis 2 7.679 0.54 Transformation Ln(x + 1) Cochran's C-test = 0.1462 Patella depressa 4 50.008 2.16 Transformation Sqrt(x + 1) Cochran's C-test = 0.0843 Patella vulgataa 4 293.129 2.77 Gibbula umbilicalis 4 9.068 0.81 Transformation Sqrt(x + 1) Cochran's C-test = 0.0908 a Osilinus lineatus 4 436.907 1.45 Nucella lapillusa 2 53.363 4.76 Siphonaria pectinata 2 14.515 4.84 Transformation Ln(x + 1) Cochran's C-test = 0.1431 a

Site

Residual

P

df

MS

F

P

df

MS

F

P

df

MS

ns

10

10.621

8.47

b0.01

30

1.253

3.03

b0.01

90

0.413

ns

6

14.239

12.21

b0.01

18

1.166

2.66

b0.01

108

0.439

ns

10

23.200

3.12

b0.01

30

7.432

4.71

b0.01

180

1.577

ns ns

10 10

105.733 11.182

22.3 6.54

b0.01 b0.01

30 30

4.742 1.710

0.70 1.63

ns b0.05

180 180

6.762 1.048

ns ns ns

10 6 6

300.387 11.222 3.002

4.94 0.99 2.45

b0.01 ns ns

30 18 18

60.862 11.393 1.225

4.39 1.60 2.88

b0.01 ns b0.01

180 108 108

13.858 7.137 0.425

Variances heterogeneous.

O. lineatus. These species showed low variability among regions and this suggests that the differences on SST among studied regions are not the main factor shaping the abundance of these species along the Atlantic coast of the Iberian Peninsula. This result was supported also by the non significant correlation between the abundance of these species and SST. Therefore, despite the important SST gradient along the Iberian Peninsula, the main factor responsible for WWS abundances seems to act at the scale of meters for P. depressa and G. umbilicalis and at the scale of shore (10s of km) for M. neritoides and O. lineatus. The distribution range observed for these species fits well with previous records made by Hidalgo (1917) and Nobre (1940). Therefore, we have not detected any significant change on their range of distribution at the Atlantic coast of the Iberian Peninsula. This result contrasts with the recent changes on the range of distribution and abundance recorded for some of these species in the U.K. (Mieszkowska et al., 2006, 2007). However, these species are distributed from Ireland (Norway for M. neritoides) to the North Atlantic coast of Africa, including Madeira and Canary Islands (Southward et al., 1995). Therefore, the Iberian Peninsula is their centre of distribution and these species were expected to expand their range to the north (Mieszkowska et al., 2006, 2007) and show range shifts on their southern limit (North of Africa) as response to the increase in SST. Alternatively, on their centre of distribution (i.e. Iberian Peninsula) changes on their abundance and other population traits could be expected. Unfortunately, no quantitative data are available about the abundance of these species during the last century, although Melarhaphe neritoides and the trochids G. umbilicalis and O. lineatus were considered very common or extremely abundant along the Portuguese coast during the past century (Gaudencio and Guerra, 1986; Hidalgo, 1917; Nobre, 1940). Recently, Boaventura et al. (2002) provide quantitative data for the abundance of P. depressa along the Portuguese coast. Quantitative data recorded by Boaventura et al. (2002) are similar to our results, with densities of 20-60 individuals per 0.25 m 2 in northern Portugal but showing higher and more variable values in the centre and south of Portugal. The lack of changes on the abundance or on the distributional range of the WWS suggests that SST along the studied area is still far from the lethal or sub-lethal temperature values for these species. The sub-tropical pulmonate false limpet, S. pectinata, showed a similar spatial pattern than WWS with low variability among regions and high variability at the scale of metres. However, this species has suffered significant changes on its range of distribution in the last century. Hidalgo (1917) reported this species at the southern Spanish Atlantic coast. Later, this species was found as common in the south and centre of Portugal (Nobre, 1940); alive specimens could not, however, be found further to the North of Buarcos (centre of Portugal). In the late 60s and early 70s, Rolán (1983) found a small population of S. pectinata

(about 40 individuals) near the border of Portugal and Galicia. This population seemed to originate from larvae that had arrived and settled there under unusual favorable oceanographic conditions; nevertheless, they did not manage to constitute a viable population in reproductive terms (Rolán, 1983). Few years later, these specimens had disappeared (Rolán, 1983) and no specimen was found during our sampling at those locations. However, we found populations of S. pectinata in Moledo, about 185 km north from the locations studied by Nobre (1940) and 30 km south than those reported by Rolán (1983). Furthermore, sizes of individuals suggest that some of those are likely several years old (Ocaña and Emson, 1999); abundant egg masses were also found close to these specimens. These observations suggest that these populations could be stable in time and produce offspring. The viability of these populations needs, however, to be further investigated because larvae might be released but those, for example, might not settle or recruit successfully depending on the environmental conditions prevailing after establishment of the original population. The significant correlation found between SST and the abundance of S. pectinata points out that the range expansion of this species could be related with SST increase. Similar range expansion of other sub-tropical species, that have their northern limit of distribution on the Atlantic Iberian Peninsula such as Patella rustica Linnaeus, 1758 or Stramonita haemastoma (Linnaeus, 1766) have been recently recorded and related to the increase in SST (Lima et al., 2006; Souto et al., 2008). Results of the present study showed a very different picture for CWS that reach their southern limit of distribution on the south Atlantic Portuguese coast. The limpet, P. vulgata, was present at all shores but always in much lower densities than the warm-water limpet P. depressa. Furthermore, there was an increase on the abundance of P. vulgata from the south to the north. These patterns were also reported by Guerra and Gaudencio (1986) and Boaventura et al. (2002). Densities of P. vulgata recorded by Boaventura et al. (2002) were similar in general terms to those found in the present study; higher densities were, however, found at CM in our study. On the other hand, the southern limit of distribution of P. vulgata was found to be the same as that reported by Fischer-Piétte (1960). However, P. vulgata showed a significant negative correlation with SST and the largest variability at the scale of region. These results could be interpreted as an early stage of the response of P. vulgata to the increase on SST. The periwinkle, L. saxatilis, and the dog whelk, N. lapillus, are also CWS that reach their southern limit of distribution in the south of Portugal. On this study, these species were only found at NP, CM and AM. These two species showed low variability among regions and high variability among quadrats as most of the studied species. However, changes on their range of distribution were found. These species were considered common along the Atlantic Iberian Peninsula by Hidalgo (1917) and Nobre (1940) but our results showed that nowadays they are only present at the northern regions (NP, CM and AM), retracting about 400 km

M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

70

70

Melarhaphe neritoides

60

60

50

50

40

40

30

30

20

20

10

10 Region

Variance(%)

Littorina saxatilis

0

0

50

7

Shore

Site

Region

Residual 50

Patella depressa

40

40

30

30

20

20

10

10

Shore

Site

Residual

Shore

Site

Residual

Site

Residual

Site

Residual

Patella vulgata

0

0 Region

Shore

Site

Region

Residual

80 Gibbula umbilicalis

40 Osilinus lineatus

60

30

40

20

20

10

0

0 Region

Shore

Site

Region

Residual 70

100 Nucella lapillus

Shore

Siphonaria pectinata

60 80 50 60

40

40

30 20

20

10 0

0 Region

Shore

Site

Residual

Region

Shore

Fig. 4. Univariate estimates of variance associated with each spatial scale in percentage of contribution for each target species.

northern. In fact, a reduction and expansion in the distribution range of these species on the studied coast had been previously reported and it was suggested to be likely due to climate change (Fischer-Piétte, 1955, 1960). The significant negative correlation that we found between SST and the abundance of these species points out that the range retraction of this species could be related with SST increase. During sampling, we also noticed the absence of the periwinkle, L. littorea, which is a common CWS in other areas. Hidalgo (1917) and Nobre (1940) reported L. littorea as abundant on the Portuguese and Spanish Atlantic coasts, mostly on intertidal rock surfaces. Nevertheless, later sampling showed that its abundance at intertidal rocky shores had decreased and in many areas

it was absent from rocky shores and restricted to estuarine habitats (Fischer-Piétte, 1963). Our study also considered L. littorea as target species but only two individuals were found, specifically among fucoid macroalgae at Viana (NP). Therefore, it seems that nowadays L. littorea is almost completely absent on the exposed rocky shores of the Iberian Peninsula and apparently restricted, when present, to hard or soft bottoms in sheltered estuaries or similar environments such as the Galician rias (Authors obs.). The observed reduction on the range of distribution of these CWS and the range expansion of S. pectinata, seem to be related to the increase of SST recorded on the study area during the last century. These shifts can

8

M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

80

Melarhaphe neritoides

r = 0.11, ns

Abundance (N 0.25 m-2)

Abundance (N 0.01 m-2)

500 400 300 200 100 0

17

18

19

18

19

20

Patella vulgata

r = − 0.42, P< 0.001

80 60 40 20

15

10

5

0 17

18

19

20

16 50

Gibbula umbilicalis

17

18

19

20

18

19

20

18

19

20

Osilinus lineatus

r = − 0.10, ns

Abundance (N 0.25 m-2)

r = − 0.07, ns 40 30 20 10

40 30 20 10 0

0 16 25

17

20

Patella depressa

16

Abundance (N 0.25 m-2)

20

16

0

17

18

19

20

16 70

Nucella lapillus

r = − 0.77, P< 0.001

Abundance (N 0.25 m-2)

Abundance (N 0.25 m-2)

40

r = − 0.16, ns

100

50

60

20

Abundance (N 0.25 m-2)

Abundance (N 0.25 m-2)

120

r = − 0.74, P< 0.001

0 16

140

Littorina saxatilis

20 15 10 5 0

17

Siphonaria pectinata

r = 0.52, P < 0.001

60 50 40 30 20 10 0

16

17

18

19

20

Temperature (oC)

16

17

Temperature (oC)

Fig. 5. Spearman rank correlations (r) for the relationship between temperature and abundance of the studied species (n = 225).

be explained by the effect of high SST; increasing the recruitment and adult survival of S. pectinata but, with opposite effects on CWS. However, laboratory experiments showed that lethal temperatures for CWS such as N. lapillus, P. vulgata or L. littorea were similar to those affecting WWS, for instance O. lineatus, G. umbilicalis or P. depressa (Evans, 1948; Sandison, 1967). Lethal water temperatures were determined around 40 °C, although the studied species cease movement or suffer coma heat at lower water temperatures, i.e. around 30 °C (Clarke et al., 2000;

Evans, 1948; Sandison, 1967). Therefore, both WWS and CWS can tolerate higher water temperature than those likely experienced by them at any of the studied regions. Moreover, Sandison (1967) found that CWS like L. saxatilis, L. littorea and N. lapillus had similar lethal and sub-lethal temperature values under aerial or submersed conditions. These species exposed to air or water temperatures around 30 °C entered in heat coma and die at temperatures around 40 °C. Air temperature of 30 °C can be easily found at some of the studied regions (especially at SP and MP)

M. Rubal et al. / Journal of Sea Research 77 (2013) 1–10

and thus, CWS could be exposed to thermal stress resulting in sub-lethal effects during low tide. The combination of elevated high air and SST resulted in high mortality of Mytilus edulis L. close to its southern limit at western Atlantic coast (Jones et al., 2010). In this way, a recent study by Beukema et al. (2009) concluded that elevated temperatures negatively affect population dynamics of the CWS bivalve Macoma balthica (L.) in a number of ways (i.e. via recruitment, mortality as well as growth) and these negative influences were observed already far below the upper lethal temperature of the species range. Moreover, Jansen et al. (2007) found that individuals of M. balthica translocated back to north Spain had elevated maintenance rates that led them to a significant reduction on the condition index; this was due to short-term but frequent exposures to sub-lethal temperatures and proposed that these mechanisms may explain the disappearance of this species from the north of the Iberian Peninsula during the last four decades (Jansen et al., 2007). Considering the qualitative and quantitative data available, we conclude that WWS with their centre of distribution on the studied area did not suffer significant changes on their abundance or distributional range. Moreover, abundance of WWS was not correlated with SST. However, sub-tropical species has increased considerably its distribution range and the CWS showed the inverse pattern at the Atlantic Iberian Peninsula coast. These changes were especially important for L. littorea that is almost absent from the studied rocky shores of the Iberian Peninsula. Therefore, species with their boundary range of distribution at coast of the Iberian Peninsula are responding to the effect of global warming similarly than at higher latitudes (Mieszkowska et al., 2006, 2007), the Atlantic coast of USA (Jones et al., 2010) or South-Eastern Pacific (Rivadeneira and Fernández, 2005). The energetic cost of frequent exposures to sub-lethal temperatures seems to be the more plausible mechanism responsible for these shifts on range distribution of CWS. On the other hand, the increase of SST seems to facilitate the recruitment and survival of sub-tropical species. Further experimental work will be needed to test these models in order to provide the knowledge to understand effects of global warming in intertidal biodiversity. Acknowledgments This study was partially funded by the project IBEROMARE — Multipolar centre for the valorisation of marine resources and residues funded by QREN through the Cooperation Program between Spain and Portugal. We are deeply grateful to Dr. João Castro and Dr. Teresa Cruz for their hospitality on the Marine Biological Station of Sines (Portugal). We thank to Dr. Celia Besteiro for providing us valuable bibliography. During this study M. Rubal (SFRH/BDP/81567/2011) and P. Veiga (SFRH/BPD/81582/2011) were supported by postdoctoral grants awarded by Fundação para a Ciência e Tecnologia (FCT, Portugal). We are also grateful to the handling editor Dr. Judi Hewitt and two anonymous referees for all the helpful comments and suggestions, which greatly improved this paper. References Allen, A.P., Brown, J.H., Gillooly, J.F., 2002. Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science 297, 1545–1548. Ardré, F., 1971. Contribution à l'étude des algues marines du Portugal II. Ecologie et Chorologie. Bulletin du Centre d'Etudes et de Recherches Scientifiques Biarritz 8, 359–574. Beukema, J.J., Dekker, R., Jansen, J.M., 2009. Some like it cold: populations of the tellinid bivalve Macoma balthica (L.) suffer in various ways from a warming climate. Marine Ecology Progress Series 384, 135–145. Boaventura, D., Ré, P., Cancela da Fonseca, L., Hawkins, S.J., 2002. Intertidal rocky shore communities of the continental Portuguese coast: analysis of distribution patterns. Marine Ecology 23, 69–90. Brierley, A.S., Kingsford, M.J., 2009. Impacts of climate change on marine organisms and ecosystems. Current Biology 19, 602–614. Burrows, M.T., Schoeman, D.S., Buckley, L.B., Moore, P., Poloczanska, E.S., Brander, K.M., Brown, C., Bruno, J.F., Duarte, C.M., Halpern, B.S., Holding, J., Kappel, C.V., Kiessling, W., O'Connor, M.I., Pandolfi, J.M., Parmesan, C., Schwing, F.B., Sydeman, W.J., Richardson,

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