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Global Change Biology (2007) 13, 2592–2604, doi: 10.1111/j.1365-2486.2007.01451.

Do distributional shifts of northern and southern species


of algae match the warming pattern?
F E R N A N D O P. L I M A *w z, P E D R O A . R I B E I R O *z, N U N O Q U E I R O Z *z,
S T E P H E N J . H A W K I N S z§ and A N T Ó N I O M . S A N T O S *w
*CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661 Vairão, Portugal,
wDepartamento de Zoologia-Antropologia, Faculdade de Ciências da Universidade do Porto, 4099-002 Porto, Portugal,
zMarine Biological Association of the United Kingdom, Plymouth, UK, §School of Oceanographic Sciences, University of Wales,
Bangor, Anglesey, UK

Abstract
Well-documented changes in species abundances and distributions coinciding with
global warming have been increasing during recent years. A trend of raising sea-surface
temperature has also been observed along the Portuguese coast which could affect
intertidal species’ ranges. The present study aimed at evaluating the direction and
intensity of distribution changes of macroalgae in the area. The last 50-year trend of
coastal air and sea temperature was reassessed, providing an accurate estimate of the
warming process. Information on species’ range shifts was obtained by comparing data
from recent resurveys with historical records of algal distributions collected during the
1950s and 1960s. Although a prevalence of northward migrations was anticipated, this
work showed a marked difference in the average direction of changes between cold- and
warm-water species. Cold-water species, when considered together, showed no particular
shifting trend, because the number of species that shifted north or south was the same.
Contrarily, all shifting warm-water species expanded their range northwards. Therefore,
generalizations about poleward range shifts due to increasing temperature should be
made with caution.
Keywords: air temperature, biogeography, climate change, intertidal macroalgae, Portugal, range limit,
rocky shores, sea surface temperature

Received 21 December 2006; revised version received 3 July 2007 and accepted 23 July 2007

geographic regions, for many species’ ranges (e.g. Sten-


Introduction
seth et al., 2002; Parmesan & Yohe, 2003; Root et al., 2003;
The distribution of species within and across ecosys- Hickling et al., 2006), and marine organisms are no
tems is ultimately determined by the environment exception (e.g. Southward et al., 1995; Sagarin et al.,
(IPCC, 2001; Clarke, 2003). There have been significant 1999; Zacherl et al., 2003; Perry et al., 2005).
responses of the Earth’s biota to recent warming (e.g. Intertidal communities are attractive for studying
Parmesan, 1996; Hughes, 2000). Perhaps the most per- climate-driven community changes due to several rea-
vasive changes documented in biological systems are sons. Generally, intertidal species respond more rapidly
the shifts in geographical ranges of species (Parmesan & than their terrestrial equivalents to environmental
Yohe, 2003; Rivadeneira & Fernández, 2005). The forth- changes because they usually have a shorter life-span
coming climatic changes, which are expected to increase associated with sessile adult stages (Southward et al.,
in strength, will act even more strongly on these limits 2004). More importantly, they are periodically exposed
(IPCC, 2001). The poleward movement in latitude or to temperature and weather extremes, and different
upperward in altitude has been observed, in different studies have shown that many intertidal species live
close to their thermal tolerance (e.g. Helmuth et al.,
Correspondence: Present address: Fernando Pádua Silva e Lima, 2002; Tomanek & Helmuth, 2002). Furthermore, recent
School of Biological Sciences, University of South Carolina, SC works suggest that even when temperatures are not
29208, USA, tel. 1 1 803 777 3936, fax 1 1 803 777 4002, sufficiently high to directly cause the death of the
e-mail: fplima@biol.sc.edu, fplima@gmail.com organisms (Denny et al., 2006), they may have sublethal
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LONG-TERM ALGAL COMMUNITY CHANGES 2593

effects that eventually lead to death, limit growth and the climate warming. Recent surveys suggest that in the
reproduction (Breeman, 1988; Somero, 2002), increase last decades significant changes have occurred, with
the susceptibility to diseases or indirectly set limits on some cold-water species disappearing from large
distribution by determining the outcome of biotic inter- stretches of coastline and warm-water species coloniz-
actions (Sanford, 1999, 2002). For these reasons, inter- ing new areas (e.g. Lima et al., 2006). These changes
tidal species have been regarded as sensitive early were correlated with the increase in sea surface tem-
warning systems for the impacts of climate change perature (SST), which off West Portugal has revealed a
(Barry et al., 1995; Southward et al., 1995; Thompson steady year-round increase from 1941 onwards, aver-
et al., 2002; Hawkins et al., 2003; Harley et al., 2006). aging more than 0.01 1C yr1 in coastal waters (Lemos &
Furthermore, surveys of intertidal organisms can be Pires, 2004; Lemos & Sansó, 2006). Air temperature
easily made because they are generally conspicuous, values have also been shown to be increasing (Klein
slow moving or sedentary, and their ranges are roughly Tank et al., 2002). Still, a comparative study involving a
one-dimensional, conveniently defined by the coastal high number of species that addresses the hypothesis of
endpoints (Sagarin & Gaines, 2002b). a prevalence of northward migration on both cold- and
While there is considerable evidence that species are warm-water species is missing.
expanding to higher latitudes in association with cli- The present work focused on the highly diverse
mate warming, there is less evidence that they are group of macroalgal species inhabiting the Portuguese
retreating at their southern range margins (Parmesan rocky coast. The most comprehensive and detailed
et al., 2005; Wilson et al., 2005). This is an issue that study of algal biogeography along this region was made
remains unclear because it is hard to know if the by Ardré (1970, 1971) during the 1950s and 1960s, in
southern populations are really more resilient to the which more than 20 sites were exhaustively surveyed.
effects of climate warming or if this difference is only The total number of taxa identified and mapped largely
apparent due to a lack of comprehensive studies exceeded 350 species, varieties and forms, from the
focusing on the low-latitude range margins of species largest Phaeophyceae to the smallest filamentous algae.
(see Franco et al., 2006). For example, in the North- The direction and intensity of macroalgae distributional
East Atlantic there are extensive long-term records of changes along the Portuguese coast was examined by
modifications in the range of intertidal species which contrasting historical records of more than 120 conspic-
have been used to judge biological responses to climate uous species with data from recent surveys. Moreover,
change (see Southward et al., 2004; Helmuth et al., 2006, Ardré (1971) empirically identified a distinct biogeo-
for a review). However, generalizations about responses graphical discontinuity (a region of significant change
to climate change made in some of these studies might in terms of macroalgal species) in central Portugal, near
be imprecise or biased given that most focused primar- the Tagus estuary, by overlapping distributions of spe-
ily on northern range limits. cies with range limits within the Portuguese coast. The
It has long been known that the Portuguese coast is at hypothesis that this discontinuity shifted northwards
an interface between cold- and warm-water intertidal with current warming was tested. The past 50-year
faunas and floras (Santos, 2000; Boaventura et al., 2002; trend of coastal air and sea temperature was reassessed
Pereira et al., 2006). A considerable number of cold- in a monthly basis to provide an accurate description of
water species (i.e. species abundant in Northern Eur- the warming process.
ope) and many warm-water species (i.e. species that are
commonly found in the Mediterranean Sea and in
Material and methods
Northwestern Africa) reach their southern or northern
distributional limits in this stretch of coastline, respec-
Temperature trends
tively. Not only the distributional ranges have been
studied since the middle of the 20th century (e.g. SST along the Portuguese coast, between January 1950
Fischer-Piétte, 1963; Ardré, 1970), but also a consider- and December 2000, was derived from in situ raw data
able number of species have been described as having obtained from the International Comprehensive Ocean–
strong latitudinal abundance clines within this area Atmosphere Data Set (ICOADS, Woodruff et al., 1988).
(Ardré, 1970; Santos, 2000; Boaventura et al., 2002). To avoid bias due to different daytime measurements,
Furthermore, shifts in the distribution of species have only data from 12:00 hours were used. Point data were
been described for this and for the flanking regions imported into GRASS Geographical Information Sys-
along the Iberian Peninsula (Fischer-Piétte, 1955, 1956, tem (GIS) (GRASS Development Team, 2006) and trans-
1957a, b). These data provide a comprehensive histor- formed into raster maps with a spatial resolution of
ical support to studies aiming at the description of 4 km cell1 using a surface interpolation method. Each
changes in distribution or in abundance related with cell was derived from the 12 nearest data points using
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2594 F . P. L I M A et al.

the distance squared weighting algorithm (Jarvis & computed using a restricted randomization technique
Stuart, 2001). Near-surface air temperature (NSAT) (a one-dimensional equivalent of a toroidal shift) to
monthly averaged data from 1950 to 2000 covering avoid bias due to possible data autocorrelation (Fortin
European land surface at 10 min resolution was ob- & Jacquez, 2000). Results from consecutive window
tained from the CRU TS 1.2 data set, available from sizes allowed the definition of regions where the highest
the Tyndall Centre for Climate Change Research (Mitch- number of significant results was observed along the
ell et al., 2002, 2004). data series. These identified zones where species sub-
The 612 (51 years  12 months) SST and 612 NSAT stitution was greater, indicating the location of biogeo-
maps were stored in GRASS GIS as monthly layers and graphical discontinuities (or regions of change in
sampled along the Portuguese coastline at regularly species composition). Although two versions of Ardré’s
spaced (10 km) points. The resulting data for each data were published (Ardré, 1970, 1971), the latter was
parameter were combined in a table where each row used because it featured information on the abundance
denoted a geographical location and each column a of species, even though in a subjective scale (absent,
month/year combination. These data were used to observed, rare, common, very common). The levels
produce general plots of the annual average tempera- ‘absent’ and ‘observed’ (one individual) were unambig-
ture change through the last 50 years. To obtain a more uous. For the remaining levels, percentage cover inter-
precise picture of the warming trend in the past 50-year vals were used (rare: o5%; common: 5–25%; very
period, monthly averages of coastal air and sea tem- common: 425%) based on the few quantitative esti-
perature were gathered for eight stations spaced along mates made by Ardré (1971) for some conspicuous
the coast (Fig. 1). Additionally, GIS was used to com- species.
pute individual warming trends for each month along After objectively locating the historical discontinuity,
the Portuguese coast at a resolution of 10 km. This the same SMW methodology was applied to contem-
procedure was necessary to verify if the warming trend porary data. However, Ardré’s sampling could not
was consistent among months or seasons. For each be precisely replicated. Although most locations visited
combination of cell/month a simple linear regression by Ardré were resurveyed between 2001 and 2006, not
between temperature and time (50 years) was com- all could be revisited because some sites simply dis-
puted. The resulting slope values were used to build a appeared, mainly due to coastal development (e.g.
surface plot of cells vs. months. Peniche, Outão and Sines). To avoid possible bias in
the SMW results caused by the mismatch between the
number and position of locations in the two sets, the
Analysis of species abundances
nearest rocky shores were reassessed during the 2001–
To verify whether the current warming could be affect- 2006 survey (Fig. 1). Therefore, original site ordination
ing species abundance/occurrence and therefore was maintained and geographical distances between
altering the location of the main biogeographical locations were hardly affected. Ardré’s semiquantita-
discontinuity in the Portuguese coast detected by Ardré tive abundance scale was also adopted to contemporary
(1971), the first step was to objectively identify its data to obtain comparable values. After considering the
historical location using Ardré’s original data. A mod- time and taxonomic expertise that a full species study
ified version of the split moving window (SMW) meth- would require, only easily identifiable and conspicuous
od (Webster, 1973; Cornelius & Reynolds, 1991) was species were resurveyed, thus reducing the algal check-
developed for this purpose. The method requires in- list for comparison to a subset of 129 species.
formation on species abundances at several locations
along a linear transect. Therefore, the coastline was
Analysis of range shifts
‘linearized’ preserving real distances among sampling
sites. A window with a specific size was placed at the From the 129 species used in the previous analysis, 39
beginning of the data series, splitting it in two equal were selected for the analysis of range shifts according
halves and recording the locations inside each half. A to the location of their distributional boundaries. A first
multivariate measure of dissimilarity (Bray–Curtis) was group consisted of species with an absolute range limit
computed between every possible pair of samples from in the Portuguese coast (like Himanthalia elongata which
different halves and the values of all comparisons were cannot be found further south or Sargassum flavifolium,
then averaged. The value obtained was assigned to the not found toward the north). Another group encom-
center of the window, which then moved one step passed species which had their absolute range limit
forward. This process was repeated until the window outside the Portuguese coast, but that displayed a
reached the end of data series. Statistical significance distributional gap in this area. This unusual situation
of dissimilarities for each window’s midpoint was may be caused by particular hydrographical features in
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LONG-TERM ALGAL COMMUNITY CHANGES 2595

Porto (Douro)

Berlengas

Cabo Carvoeiro

Lisbon
Tagus

50 km

Fig. 1 Study area with rocky coast depicted in bold. The two major cities (Lisbon and Porto) and the respective river mouths (Tagus and
Douro) are shown for reference. Locations sampled for climatic data are represented by white arrows. White circles represent locations
visited only by Ardré (1970) in the 1950s and 1960s. Black circles correspond to locations only surveyed in 2001–2006. Grey circles
represent locations visited in both periods.
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2596 F . P. L I M A et al.

the Eastern Atlantic Coast, such as cold upwelling areas during the low spring tides between 2001 and 2006.
in North-Western France, Northern Portugal and Mor- More than 50 locations were selected covering the entire
occo, and warm areas in the Bay of Biscay and Southern continental Portuguese rocky coast (Fig. 1), thus provid-
Portugal (OSPAR, 2000; Sanchez & Relvas, 2003; Lima ing accurate data on extant distribution limits. To objec-
et al., 2006). For example, Fucus vesiculosus and Bifurcaria tively identify significant changes in distribution
bifurcata have their southern boundary in Morocco, endpoints, the methodology proposed by Rivadeneira
where the temperature is still cold enough to sustain & Fernández (2005) was adopted. Coastline distances
populations, but cannot be found in the warmer south- were linearized and distances between every pair of
ern Portugal. On the other hand, Padina pavonica and adjacent locations measured. These distances were used
Codium adhaerens are abundant in Northern Spain and as null expectation because they reflect the level of
South-Western France, but are absent from the colder sampling error for which changes can be assessed.
region of Northern Portugal. Together, these two groups Therefore, only shifts greater than the percentile 95
comprised 25 cold- and 13 warm-water species, for (38.6 km) of the distance distribution were considered
which changes in the distributional limits in the Portu- significant.
guese coast could be correlated with environmental
warming. Additionally, the nonnative species Sargassum
Results
muticum, which has been spreading from the north
during the last decades, was also surveyed. The classi-
Temperature trends
fication of species into cold- or warmer-water groups
was based on their historical distribution along the A consistent increase in sea temperature was observed
coasts of Europe and North Africa, and on the presence throughout the entire Portuguese coast (Table 1). The
of southern or northern distribution limits on the Por- slopes of all linear regressions were statistically signifi-
tuguese coast (Ardré, 1970, 1971; Luning, 1990; Guiry & cant except for Faro, which is the southernmost loca-
Guiry, 2006). For each one of the selected species, all tion. SST warming rates ranged from 0.0009 to
available historical records of their range boundaries 0.0015 1C month1 and the average temperature in-
in Portugal were considered, even if the locations crease in the eight localities over the 50-year period
were not visited by Ardré herself. Thus, the use of was 0.74 1C. With the exception of short cold pulses in
several complementary historical studies (Miranda, the mid-1960s, 1970s and mid-1990s, SST rose continu-
1934; Palminha, 1951; Dizerbo, 1954a, b; Ardré, 1957; ally with the main warming period occurring during
Fischer-Piétte, 1958; Rodrigues, 1963) allowed an accu- the last decade (Fig. 2a). On the other hand, monthly
rate placement of historical range limits. Abundance NSAT revealed a higher variance over the time series
details were discarded, because the only required in- and the increases in monthly temperature were not
formation was the southernmost (cold-water species) or significant in any of the eight localities analyzed. In this
northernmost (warm-water species) locality where each case, a stronger predominance of the cooling phase was
seaweed was found. observed during the 1960s and the 1970s. Nevertheless,
Contemporary range limits were assessed by thor- the overall trend was similar to that recorded for the
oughly surveying a considerable number of localities SST, with a major period of warming in the late 1990s

Table 1 Warming trends (expressed by the slope of OLS regression) of sea surface temperature (SST) and near-surface air
temperature (NSAT) at eight coastal locations along the Portuguese coast

SST NSAT

Slope Slope
Location Latitude Longitude (1C month1) P (1C month1) P

Moledo do Minho 41.87561N 8.88031W 0.0012 0.008 0.0016 0.075


Douro estuary 41.14821N 8.68201W 0.0012 0.009 0.0016 0.078
Figueira da Foz 40.13161N 8.87191W 0.0014 0.002 0.0014 0.131
Peniche 39.36451N 9.40981W 0.0015 0.000 0.0011 0.227
Tagus estuary 38.66011N 9.29671W 0.0013 0.001 0.0010 0.282
Sines 37.93791N 8.87681W 0.0012 0.004 0.0015 0.122
Sagres 36.99411N 8.94891W 0.0013 0.003 0.0012 0.123
Faro 36.96081N 7.92541W 0.0009 0.058 0.0016 0.110

Locations can be found in Fig. 1. Data range from January 1950 to December 2000. Significant slopes are depicted in bold.

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LONG-TERM ALGAL COMMUNITY CHANGES 2597

North North

PORTUGAL

SPAIN

18.5 °C 19.0 °C

15.5 °C 13.0 °C
(a) (b) (c)
South South
1950 1960 1970 1980 1990 2001 1950 1960 1970 1980 1990 2001

Fig. 2 Yearly averaged sea surface temperature (a) and near-surface air temperature (b) along the Portuguese coastline from January
1950 to December 2000. (c) Location of discontinuities after split moving window analyses. White arrow indicates the discontinuity
identified using Ardré’s complete data set. Black arrow indicates the discontinuity identified using Ardré’s subset data and gray arrow
indicates the discontinuity identified with contemporary data.

North

PORTUGAL

SPAIN

1.53 °C

− 0.51 °C

South
Fev Apr Jun Aug Oct Dec

Fig. 3 Monthly sea surface temperature rate of change (1C) per 50 years (1950–2000). The vertical axis represents the Portuguese coast.

(Fig. 2b). The warming trend was not homogeneous values were observed from July to September, where
between months (Fig. 3). Increases were much more average SST increased up to 1.53 1C, much more than
pronounced during winter and summer. The highest the average increase of 0.74 1C in the 50-year period.
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2598 F . P. L I M A et al.

Table 2 Number and direction of changes in range bound- among them. Half of the species shifted northwards
aries of selected species and the other half southwards. Globally, shifts in end-
points varied from 59 to 583 km with a mean value of
Cold-water Warm-water
235 km. The distance traveled by northward shifting
Direction of shift species species Total
species did not differ from those shifting southward
Northwards 7 8 15 (t-test, t 5 0.872, df 5 13, P40.05).
Southwards 7 0 7
No significant change 12 5 17
Total 26 13 39 Discussion
It is known that environmental conditions are major
determinants in shaping species ranges (Gaston, 2000;
Walther et al., 2002; Clarke, 2003). Species abundances
Species abundances are thought to be inversely proportional to the strength
of adverse factors (Sorte & Hofmann, 2004), which are
SMW analysis successfully detected significant distribu-
often assumed to be weaker at the middle of their range
tional discontinuities in the three tested data sets (two
and stronger near the distribution limits. Some authors
historical and one contemporary). The first analysis,
have shown that this is not always true, especially in
performed on Ardré’s complete species list, revealed a
the intertidal habitat, because regional variations in
clear discontinuity in central Portugal, at the Tagus
coastal temperature (due to upwelling, for example)
estuary (Fig. 2c). The discontinuity was detected at
are frequently strong enough to disrupt the monotonic
window scales ranging from 300 to 400 km. On the
temperature cline along the coast (Sagarin & Gaines,
other hand, the analysis using Ardré’s subset data gave
2002a, b; Sagarin & Somero, 2006). However, the analy-
a different result. In this case, the discontinuity was
sis of the temperature patterns off the Portuguese coast
detected near São Pedro de Moel, approximately 197 km
revealed a clear latitudinal gradient in temperature
north of the Tagus mouth, at window scales of 50–
throughout the whole year and the intense upwelling
300 km. Hence, the location of the historical discontinu-
during the warm season only contributes to sharpen
ity varied with the data set considered. The analysis of
that gradient (Lima et al., 2006). Therefore, under a
the contemporary data set identified a discontinuity
linear temperature gradient, poleward range shifts of
roughly at the same position as the one found using
both northern and southern species caused by a warm-
Ardré’s subset data (Fig. 2c).
ing climate were likely to occur.
The sea and air temperature are naturally highly
variable over space and time. Owing to the density
Range shifts
and specific heat of seawater, the ocean is more resilient
The analysis of range shifts revealed a significant rate of to changes in temperature than the atmosphere which
change among species, which differed from the random shows higher short-scale variability (Levitus et al.,
expectation of zero (one-sample t-test, t 5 5.520, df 5 36, 2000). The absence of a significant trend for the NSAT
Po0.05). Additionally, more than half of the studied of coastal sites may have been caused by a longer
species (22 out of the 39) displayed a significant dis- cooling period during 1970–1980, which obscured the
placement in their range limit (i.e. more than the effects of a noticeable increase in the last decade. Con-
38.6 km threshold; Table 2). The remaining 17 species trarily, rates of change in ocean temperature were sig-
exhibited no shifts at all (with the current range bound- nificant and similar to those already reported by Lemos
ary coinciding with the historically reported location) or & Pires (2004) and Lemos & Sansó (2006) for coastal
the shifted distance was smaller than the assessment Portuguese waters. Moreover, this warming rate also
error (Rivadeneira & Fernández, 2005). The complete matched the increase in SST observed in the Bay of
list of shifting and nonshifting species can be found in Biscay and the English Channel (Hawkins et al., 2003;
Table 3. From the group of southern species showing Southward et al., 2004), in the North Sea (Genner et al.,
significant shifts (62%), all were found northward in 2004; Perry et al., 2005) and in coastal North-Western
relation to their historical range limits. Apparently, Pacific (Sagarin et al., 1999). In all of these locations
these results were in agreement with the initial predic- significant changes in species distributions have been
tion of a northward dominance in migration events. On described.
the other hand, the pattern observed in the cold-water The differences between discontinuities detected by
species was quite different. In this case, 54% of the SMW analyses for Ardré’s (1971) full set and subset data
species exhibited significant shifts in their range limits, were not unexpected. Ardré (1971) observed that the
but the direction of such shifts was not consistent group of northern species whose southern limits were
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LONG-TERM ALGAL COMMUNITY CHANGES 2599

Table 3 Species for which shifts in distribution were assessed

Historical range Current range Shift


boundary References boundary (km)

Cold-water species
Shifted northwards
Chondrus crispus Sines Ardré (1971) Cabo Raso 180
Desmarestia ligulata Portinho d’ Arrábida Ardré (1971) Avencas 70
Dumontia contorta Douro estuary Ardré (1971) Amorosa 62
Himanthalia elongata S. Martinho do Porto Ardré (1971), Fischer-Piétte (1958) Labruge 219
Palmaria palmata Tagus estuary Ardré (1971) Valadares 358
Pelvetia canaliculata Berlengas Islands Palminha (1951) Cabo do Mundo 245
Phycodrys rubens Moledo Ardré (1971) species absent na
Shifted southwards
Ahnfeltia plicata Tagus estuary Ardré (1971) Martinhal 330
Bifurcaria bifurcata Tagus estuary Ardré (1971), Fischer-Piétte (1958) Monte Clérigo 257
Desmarestia aculeata Douro Ardré (1971), Rodrigues (1963) Baleal 227
Fucus vesiculosus Vila Nova de Milfontes Dizerbo (1954a) Ingrina 157
Halidrys siliquosa Pontevedra (Spain) Miranda (1934), Ardré (1957) Montedor 90
Mastocarpus stellatus Sines Ardré (1971) Monte Clérigo 121
Sargassum muticum Species absent na Almograve na
Nonsignificant shift
Ascophyllum nodosum Forte da Vigia Ardré (1971), Fischer-Piétte (1958) Forte da Vigia nc
Calliblepharis ciliata Portinho d’ Arrábida Palminha (1951) Portinho d’ Arrábida nc
Cystoseira baccata Lagos Ardré (1971) Dona Ana nc
Fucus spiralis Sagres Ardré (1971), Fischer-Piétte (1958) Martinhal nc
Laminaria hyperborea Baleal Ardré (1971) Baleal nc
Phyllophora crispa Peniche Ardré (1971) Peniche nc
Fucus serratus Forte da Vigia Ardré (1971), Fischer-Piétte (1958) Amorosa 9
Gelidium corneum Algarve Ardré (1971) Castelo nc
Laminaria saccharina Forte da Vigia Ardré (1971), Fischer-Piétte (1958) Amorosa 9
Petalonia fascia Sines Ardré (1971) Vila Nova de Milfontes 28
Delesseria sanguinea Montedor Dizerbo (1954b) Vila Praia de Âncora 9
Dilsea carnosa Douro estuary Ardré (1971) Labruge 18
Warm-water species
Shifted northwards
Asparagopsis armata S. Martinho do Porto Ardré (1971) Vila Praia de Âncora 287
Codium adhaerens Baleal Ardré (1971) S. Martinho do Porto 59
Halopithys incurva Lagos Ardré (1971) Bafureira 475
Hypnea musciformis Sagres Ardré (1971) Portinho d’ Arrábida 269
Leathesia difformis Peniche Ardré (1971) Vila Praia de Âncora 320
Padina pavonica Sesimbra Ardré (1971) Baleal 187
Sargassum flavifolium Sines Ardré (1971) Moledo 593
Valonia utricularis Tagus estuary Ardré (1971) S. Martinho do Porto 197
Nonsignificant shift
Cystoseira tamariscifolia Vila Praia de Âncora Ardré (1971) Vila Praia de Âncora nc
Scytosiphon lomentaria Peniche Ardré (1971) Baleal nc
Halopteris filicina Vila Praia de Âncora Ardré (1971) Afife 5
Amphiroa sp. Sines Ardré (1971) Vila Nova de Milfontes 28
Caulacanthus ustulatus Forte da Vigia Ardré (1971) Moledo 20

Significant shifts are depicted in bold.


na, not applicable; nc, no change.

located in the Portuguese coast included mainly large contrary, the majority of the southern species which
and conspicuous brown algae such as Himanthalia elon- displayed northern limits in this area were small and
gata, Ascophyllum nodosum or Pelvetia canaliculata. On the cryptic red algae belonging to genera such as Griffithsia,
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2600 F . P. L I M A et al.

Polysiphonia or Coelotrix. Because in the present resur- Several hypotheses can be put forward to explain the
vey small and inconspicuous species were discarded observed differences between the two groups of species.
from the analysis, the mismatch between discontinuities The simplest explanation is that their range shifts are no
was anticipated. Furthermore, Ardré (1971) reported more than chance fluctuations not differing from the
the region of Cabo Carvoeiro as a secondary, but never- random expectation. This could have happened in the
theless important, biogeographical discontinuity if only cold-water group, because the proportion of species
large species were considered, which roughly coincided shifting northwards, southwards, or not shifting did
with the discontinuity detected in SMW analysis for the not differ from chance (w2 5 1.93, df 5 2, P40.05). On
129 species subset. the other hand, in the group of warm-water species
The SMW analysis for contemporary data detected a these proportions cannot be easily explained by chance
discontinuity that coincided with the one found using alone given that the observed changes were unidirec-
Ardré’s subset data, suggesting that the observed tional (toward the north).
increase in sea-surface temperature did not caused According to van den Hoek (1982), in the North-
significant changes on the distribution of the studied Eastern Atlantic the distributional limits of most warm-
species, when analyzed at an assemblage level. It and cold-water algal species seem to be set by sublethal
should be emphasized that this conclusion is only valid effects of temperature, which prevent growth and/or
for the particular group of species resurveyed (conspic- reproduction, rather than by lethal effects. Moreover,
uous macroalgae) and, thus results should not be con- these sublethal effects would act on the two groups of
sidered out of their context. Another important aspect is species at different times. The poleward expansion of
that the maintenance of the discontinuity position does most warm-water species would be limited by the
not necessarily mean that individual ranges remained absence of suitable high temperatures during the sum-
unchanged. This result may arise from two different mer, while the equatorialward range extension of cold-
scenarios: when no changes occur or when individual water species would be hindered by the effects of warm
range limits or abundances vary but the overall changes winters (van den Hoek, 1982; Breeman, 1988). Although
are symmetrical. Providing that a change in one parti- the analysis of the long-term SST regime during the past
cular species has a correspondent and inverse change 50 years has shown a consistent increase in tempera-
in another, the average region of change will remain ture, a more detailed inspection of the data set revealed
unaltered. The SMW method is unable to distinguish that this was not homogeneous among months. In-
between these situations and caution must be taken in creases in SST were more pronounced during the winter
the interpretation of the results. and summer months, but particularly in the latter
The study of individual shifts helped to address the where the average increase was around 1.5 1C in the
question concerning the nonchanging discontinuity. 50-year period. Therefore, the observed northward ex-
However, this analysis was performed solely using pansion of several southern species is consistent with
distributional limits, meaning that any possible changes this change. On the contrary, the warming during
in abundance that might have contributed to the pre- the winter months cannot fully explain the disparate
sent discontinuity location were not taken into account. responses observed in cold-water species. These may
Apparently, the discontinuity did not move due to a exhibit differences in sensitiveness to the warming
combination of several factors, such as a low number of winter temperature, with only the most vulnerable
shifting species (only 23 out of 129) and the existence of being affected and retreating toward the north. This
opposite shifts that ended up neutralizing each other. would not be surprising, given that even among closely
The most evident feature, however, was the clear diver- related species the responses to climate may be quite
gence between shifting patterns of northern and south- different (Hodkinson, 1999). However, the counterintui-
ern species. Cold-water species, when considered tive southward expansions of cold-water species are
together, showed no particular shifting trend, because more difficult to understand. Indirect effects of the
the number of species that shifted north or south was upwelling, which is a prevalent feature of the Portu-
precisely the same. Contrarily, all shifting warm-water guese coast, are a plausible explanation. In a warming
species expanded their range northwards. Similar scenario, stronger equatorial winds originated by the
trends were already observed both by Helmuth et al. increased difference in temperature/pressure of air
(2006) in Britain, where only two northern intertidal masses over land and sea may lead to intensified
species showed contraction of their range, contrasting upwelling (Bakun, 1990; Snyder et al., 2003), cooling
with eight range expansions of warm-water species, coastal waters and thus allowing the southward expan-
and by Parmesan & Yohe (2003) in a meta-analysis sion of cold-water species, in particular those from low-
involving a wide number or range shifts in terrestrial shore or subtidal habitats, which remain immersed
species. during most of their lifetime. Nonetheless, recent
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Journal compilation r 2007 Blackwell Publishing Ltd, Global Change Biology, 13, 2592–2604
LONG-TERM ALGAL COMMUNITY CHANGES 2601

evidence does not support this hypothesis because it present results suggest that the range overlap between
shows that upwelling has been decreasing in this parti- the two groups has clearly increased, which may have
cular region (Lemos & Pires, 2004). Furthermore, the intensified biotic interactions, a topic worth further
group of cold-water species that expanded toward the investigation.
south included not only low-shore algae but also typical Several other factors not related (or indirectly related)
mid-shore species (e.g. Mastocarpus stellatus and Fucus to changes in temperature cannot be discarded as
vesiculosus). possible explanations for at least some of the observed
Another explanation for the observed differences distributional shifts. These include biotic interactions
between warm- and cold-water species is that the latter (e.g. grazing and competition), and anthropogenic ef-
are probably more resilient, tolerating longer periods of fects over the coast (e.g. pollution, coastal erosion). For
adverse conditions. In these situations they may grow example, recent evidence from transplant experiments
slower, ceasing their reproductive growth and offspring of Himanthalia elongata to its former southern distribu-
production, but might not go extinct. Moreover, if tional limit suggests that the range retreat of roughly
during the generally warming trend some cold pulses 200 km was not directly caused by the increasing SST
occur, even if only for short periods of time (as those observed off the Portuguese coast. This range shift was
observed along the Portuguese coast in SST during the more likely a consequence of increased grazing pres-
middle 1960, 1970 and 1990), then the reproductive sure or driven by competition with a major space
output of these species might be sufficient to maintain occupier, the reef-building polychaete Sabellaria alveolata
local populations and to allow them to expand toward (Lima, 2007).
the south. This phenomenon was described by South- The present findings emphasize the importance of
ward (1967) and Southward et al. (1975, 1995), who considering the synchrony between climatic oscillations
observed southward range expansions of cold-water and population dynamics (Zacherl et al., 2003) and the
intertidal barnacles associated with cooling SST pulses, need to understand single-species’ responses, which
followed by warmer periods during which these popu- when combined shape the patterns of community
lations were able to maintain their extended ranges. change (Genner et al., 2004; Gilman, 2006). Additionally,
Furthermore, differences in metabolism, which deter- results from the present work suggest that single-spe-
mine growth rates and the time required to attain sexual cies responses may be highly variable and as such
maturity or even life span may also explain some of the generalizations about poleward shifts should not be
observed patterns. It is known that warm-water species taken lightly. To accurately identify and predict com-
generally grow faster and reproduce earlier during their munity structure changes under climate change scenar-
shorter life extent compared with cold-water congeners ios, it is essential to gather and keep up to date accurate
(Lewis, 1986). Thus, it is reasonable to expect that records of a high number of species distributions.
geographical responses to climate warming will be Future studies should also address the role and the
noticed earlier on warm-water species, because their relative importance of species interactions on the dis-
life-cycle characteristics confer them a more opportu- tributional changes here described. The algal assem-
nistic character. Also, in a warming scenario, the new blages considered in this work, coupled with additional
environmental conditions will allow southern species to species whose distributional limits are in a shifting
expand their range northwards, thus releasing them process (see Lima et al., 2006), are ideal for a continuous
from competitor and predator pressures. Conversely, study, which will definitely help to build more accurate
native cold-water species still have to interact with predictive models on how species ranges are likely to
coevolved competitors, predators and diseases in addi- shift in response to global climate change.
tion to the invaders, which might decrease their fitness
(Sax & Brown, 2000). It has been shown that the
distributions of both terrestrial (e.g. Brooker, 2006) and Acknowledgments
marine organisms (e.g. Connell, 1961; Wethey, 2002) are
Authors are grateful to Dr T. D. Mitchell from the Tyndall Centre
conditioned not only by the physical environment but
of Climate Research for the climatic data provided. The ICOADS
also by biological interactions, and that the responses to data were provided by the Data Support Section of the Scientific
the environment can themselves be affected by biotic Computing Division at the National Center for Atmospheric
factors like competition and predation (Sanford, 1999, Research (NCAR). NCAR is supported by grants from the
2002; Richardson & Schoeman, 2004). An increase in National Science Foundation. F. P. Lima and P. A. Ribeiro were
competition between cold- and warm-water species is funded by FCT grants refs. SFRH/BD/8730/2002 and SFRH/
BD/8232/2002, respectively. S. J. Hawkins was funded by NERC
expected if warm-water species are shifting northwards grant in aid to the MBA the Marclim funding consortium
while cold-water species are not moving or only mov- (English Nature, Scottish Natural Heritage, Countryside Council
ing by chance both southwards and northwards. The for Wales, Environment Agency, Scottish Executive, Defra, WWF,

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Journal compilation r 2007 Blackwell Publishing Ltd, Global Change Biology, 13, 2592–2604
2602 F . P. L I M A et al.

Crown Estate). The comments of R. Xavier have contributed Fischer-Piétte E (1957b) Sur les progrès des espèces septentrio-
significantly to the quality of this paper. We also thank the nales dans le bios intercotidal ibérique: situation en 1956–1957.
suggestions of two anonymous referees that contributed to the Comptes rendus des scéances de l’Académie des Sciences, 245,
improvement of the manuscript. 373–375.
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