Functional Responses of Juvenile Kelps, Laminaria Ochroleuca and Saccorhiza Polyschides, to Increasing Temperatures

Aquatic Botany 113 (2014) 117–122

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Aquatic Botany

journa l homepage: www.elsevier.com/locate/aquabot

Functional responses of juvenile kelps, Laminaria ochroleuca and

Saccorhiza polyschides, to increasing temperatures

a,∗ a a b

Szymon Biskup , Iacopo Bertocci , Francisco Arenas , Fernando Tuya

CIIMAR/CIMAR – Centro Interdisciplinar de Investigac¸ ão Marinha e Ambiental, University of Porto, Rua dos Bragas, n.289, Porto 4050-123, Portugal

BIOGES, Universidad de Las Palmas de Gran Canaria, 35017 Las Palmas de G.C., Canary Islands, Spain

r t a b

i s

c l e i n f o t r a c t

Article history: We tested the ability of juvenile sporophytes of two coexisting kelps native to Portugal, Laminaria

Received 29 July 2013

ochroleuca and Saccorhiza polyschides, to adjust their photosynthesis and respiration to increasing sea

Received in revised form 19 October 2013

water temperatures. These responses were measured for S. polyschides from both the subtidal and the

Accepted 22 October 2013

intertidal habitat, and for L. ochroleuca from the intertidal habitat. L. ochroleuca showed a reduced ability

Available online 31 October 2013

to acclimatize to changing conditions, whereas S. polyschides demonstrated a larger physiological ﬂex-

ibility. These ﬁndings are connected with the life-history traits of these species. Additionally, optimum

Keywords:

temperatures for the primary production of kelps were assessed, indicating higher values for inter- than

Acclimatization

Productivity subtidal S. polyschides. Signiﬁcant physiological differences between inter- and subtidal S. polyschides

Respiration were observed, based on metabolic rates of primary production and dark respiration. This study sug-

Saccorhiza polyschides gests that, under a warming climate scenario, responses can signiﬁcantly vary for each species, and that

Laminaria ochroleuca L. ochroleuca is more susceptible to ocean warming than S. polyschides, due to larger acclimatization

Temperature capacity of the latter.

1. Introduction events (e.g. Lima and Wethey, 2012; Wernberg et al., 2013). Effects

of temperature changes on communities and ecosystems are well

Although environmental effects of climate change are complex known for terrestrial plants and pelagic systems (e.g. Parmesan,

and diverse, there is general consensus on increasing atmospheric 2006), while relatively few studies have explicitly examined effects

and sea surface temperatures (SST) over the past decades. Anthro- of global warming on coastal marine communities (Wernberg et al.,

pogenic activities, such as greenhouse gas emissions, are mostly 2012). Among all studies on climate-related changes in natural

considered responsible for a global average increase of SST in the communities, on the expected biological responses to tempera-

◦

last century of 0.6 ± 0.2 C (IPCC, 2007). The rate of warming is ture increases and on the eco-physiological mechanisms behind

not constant throughout the globe, creating high risk areas, which these, only 5% refer to marine systems. Nevertheless, recent stud-

include polar and cold-temperate regions. For example, SST has ies have indicated that one of the main consequences of rising

◦

risen at a mean rate of 0.27 ± 0.13 C per decade in the eastern ocean temperature is distributional range shifts of species world-

Atlantic since 1982, which is more than the global average (Lima wide (O’Connor et al., 2012). Cases of latitudinal shifts of rocky

and Wethey, 2012); importantly, the IPCC (2007) predicts a rise shore species have been documented in Europe, along the Atlantic

◦ ◦

in temperature between 2 C and 4 C in the northeast Atlantic by and Paciﬁc coasts of North America and in the southern hemisphere

2100. (Lima et al., 2007; Wernberg et al., 2011). These were considered as

The increase of temperature is potentially the most important primarily driven by changes in patterns of recruitment and survival

change occurring in the oceans in the last decades, as it inﬂuences of populations that are strongly affected by temperature (Barry

physiological and ecological processes at all biological levels, from et al., 1995).

genes to ecosystems (Kordas et al., 2011; Smale et al., 2011). In Kelp beds are key organisms across temperate rocky shores in

addition to a gradual increase in temperature, a key element of both hemispheres (Steneck et al., 2002). Being cool-water adapted

climate change is an increase in climate variability; more specif- species, they are particularly sensitive to sea temperature rise,

ically, an increase in the frequency and magnitude of warming which can negatively affect their growth, survival, reproduction

and recruitment (Wernberg et al., 2010). In the northern hemi-

sphere and under predicted warming, such effects may lead to

∗ further decreases in abundance of kelp species at their southern

Corresponding author.

E-mail address: [email protected] (S. Biskup). range edges and to their retreat northward in the near future. For

118 S. Biskup et al. / Aquatic Botany 113 (2014) 117–122

example, a trend northward shifts of kelp distribution in the past gametophytes. Male gametophytes produce sperm cells and female

decades is supported by local communities’ awareness, through gametophytes egg cells. After fertilization, these create a zygote

personal and anecdotic observations, along the entire Portuguese that develops into a new diploid sporophyte that starts a new

coastline (Assis et al., 2009). Abundant and dense kelp beds that cycle (Pereira et al., 2011). Based on the life span of the sporo-

were present along the Portuguese coast in previous decades phyte, kelp species can be identiﬁed as annual or pluriannual

(Ardré, 1971) are currently reduced to patches with irregular distri- (perennial) (Birkett et al., 1998; Pereira et al., 2011). Saccorhiza

bution (Assis et al., 2009) and almost restricted to northern Portugal polyschides (order: Tilopteridales, family: Phyllariaceae), which is

(Tuya et al., 2012). As ‘foundation species’ in temperate regions the most abundant kelp in southern Europe (Raffaelli and Hawkins,

(Wernberg et al., 2010), kelps play a crucial role in primary pro- 1996), is an annual seaweed. Its sporophyte grows quickly in

duction and habitat provision for associated biota. Moreover, the spring and summer and start decaying in autumn. Most individ-

ecological function of kelp beds might be ampliﬁed in the future, as uals are detached from the rocky substrate during winter storms.

they were shown to be able to buffer the negative effects of climate- In contrast, Laminaria ochroleuca (order: Laminariales, family: Lam-

related disturbance and mitigate environmental stress (Bertocci inariaceae) is a pluriannual alga, with a life cycle that can span up

et al., 2010; Wernberg et al., 2010). As a result, conservation of to 18 years, becoming fertile after 2–6 years (Birkett et al., 1998).

the marine environment and possible mitigation of climate change The aim of this study was to test the effects of increasing sea

will critically depend on understanding the response mechanisms water temperature on the physiological performance of juvenile

of these species to future environmental scenarios (Wernberg et al., sporophytes of the native kelps, L. ochroleuca and S. polyschides,

2012). from continental Portugal. We expected that kelps would show an

When exposed to environmental conditions outside their nor- increase in physiological responses with increasing temperatures.

mal physiological range, populations of macroalgae can react in one Furthermore, we investigated possible variation in these responses

of four possible ways: migration (dispersal toward a more favorable between both kelp species from the intertidal and between inter-

area), adaptation (selection of the phenotypic traits of individuals and subtidal sporophytes of S. polyschides. We expected some vari-

that match the new environment), extinction (algae are not capa- ability in physiological responses between these two kelp species

ble to migrate and\or to adapt; therefore, the species becomes and between habitats, due to differences in optimal temperatures,

extinct) (Clarke, 1996), or acclimatization (the organism adjusts life cycles traits of both kelps, and different conditions between the

its physiological or morphological traits to gradual changes of the inter- and subtidal. Changes in metabolic rates caused by increas-

environment, which leads to increased tolerance) (O’Connor et al., ing temperature were expected to be higher for S. polyschides than

2012). Persistence of kelp beds is often achieved through acclima- L. ochroleuca, due to the annual life cycle of the former species.

tization, which in contrast to adaptation does not involve genetic Furthermore, we expected differences in metabolism sensitivity

differentiation within species, but occurs within a lifetime of an between inter- and subtidal S. polyschides, where the former was

individual (Wernberg et al., 2010). When exposed to altered envi- expected to be less affected by adverse abiotic changes (here, SST

ronmental conditions, kelps may demonstrate resilience by altering increases), because of the natural exposure to the harsher condi-

their metabolic responses or undergoing structural changes and tions of the intertidal.

adjusting physiological processes in order to maintain efﬁciency.

In this process, organisms show a certain ﬂexibility of their

metabolism, which is however possible only to a limited extent

2. Materials and methods

of environmental changes, e.g. temperature rise (Wernberg et al.,

2010). Nevertheless, this process can have costs in terms of offset-

2.1. Distribution range of kelp species

ting some physiological constrains of kelps, including, for example,

a lower resilience of adults to concomitant perturbations, or a

The distribution range of S. polyschides stretches from the west

reduced ecological performance of recruits (Staehr and Wernberg,

coast of Norway, through the British Isles, extending along the

2009; Wernberg et al., 2010). As a consequence, exposure to ele-

western coast of the Iberian Peninsula, with the southern limit

vated temperatures, although buffered by acclimatization, will

located in the warm–temperate waters of the Moroccan coast

increase the sensitivity of kelps to other concomitant sources of

(Birkett et al., 1998; Pereira et al., 2011). The distribution range of L.

environmental pressure, such as extreme storms or reduced water

ochroleuca stretches from the British Isles in the north to the Moroc-

quality (Roleda and Dethleff, 2011; Wernberg et al., 2013). In addi-

can coast in the south (Birkett et al., 1998; Pereira et al., 2011),

tion, some species are more vulnerable than others (Roleda, 2009;

where it shares the southern distribution limit with S. polyschides

Roleda et al., 2010), due to their limited acclimatization capabilities,

(Pereira et al., 2011).

which eventually will lead to distributional range shifts and sub-

stantial changes in local communities (Graham, 2004). For example,

when acclimatization cannot buffer the negative effects of environ-

2.2. Collection of algal material

mental pressure, retreat and migration occurs, as documented for

some kelp populations on the northern coast of Spain (Fernández,

2011). Juveniles (20–25 cm of total lengh) of L. ochroleuca (n = 108) and

S. polyschides (n = 108) were collected from low intertidal areas

The coast along continental Portugal has overlapping distribu-

(between 0 m and 0.20 m above Chart Datum) and shallow sub-

tions of species of both boreal and Lusitanian origins (Lima et al.,

tidal rocky reefs (3–8 m depth) for S. polyschides (n = 108), along

2007; Tuya et al., 2012) and is included within the South European

about 20 km of coastline in northern Portugal (southernmost point

Atlantic Shelf ecoregion. A large number of cold- and warm-water

◦ ◦ ◦

of sampling: 41 37 6 N 8 49 4 W and northernmost: 41 47 2 N

marine species have their southern or northern distributional range

◦

8 53 6 W) between 21st of March and 2nd of April 2012. The sea

edges along this stretch of coastline (Lima et al., 2007), while other

◦

water temperature at the sampling locations was around 12–13 C

species show latitudinal clines in abundance (Boaventura et al.,

(Aqua MODIS SST, NASA). Collected algal material was transported

2002; Tuya et al., 2012).

to the laboratory and kept in a tank (300 l capacity, protected from

The life cycle of kelps is composed of two altering stages:

◦

excess of sun light) with aerated sea water at around 12 C. Every

a microscopic, haploid gametophyte and a macroscopic, diploid

3− 4−

two days, 30 ml of a macro-nutrients solution (NO , PO ) were

sporophyte. Mature sporophyte produces spores, which, after sett-

added to provide conditions without nutrient-limited stress.

ling on a substrate, develop into either male or female haploid

S. Biskup et al. / Aquatic Botany 113 (2014) 117–122 119

2.3. Productivity and respiration where rate 1 and 2 are metabolic rates for productivity measured at

temperatures T2 (higher temperature) and T1 (lower temperature),

Primary productivity was determined by measurement of the respectively. Q10 is the increase factor in the rate of a chemical

concentration of dissolved O2, using whole juvenile plants in reaction when temperature increases (Van’t Hoff, 1898). Because

a temperature-controlled incubation unit, with 400 W Halogen the arbitrary selection of T1 and T2 has a systematic effect on the

® ◦

Osram bulbs and neutral ﬁlters. The incubator allowed simulta- Q10 estimation, all calculations were done for each 5 C interval

◦

neous and independent measurements on algal material exposed to (from 5 C up to determined Topt) for each of the 3 cases (intertidal

−2 −1

six light intensities (0, 30, 90, 210, 710 and 1445 ␮Einstein m s ), L. ochroleuca, inter- and subtidal S. polyschides) and then the mean

covering an entire PAR light range, from light-limited conditions values were calculated as the ﬁnal, reported, Q10. In order to test

(dark incubation) to photo-inhibition; this allowed to plot con- which was the effect of supra-optimal (i.e. above Topt) temperatures

ventional photosynthesis-irradiance curves. All algal material was on productivity, the reduction above Topt was calculated the same

◦ ◦

given a short period of ∼15 min of acclimatization in the incubation way as Q10, but for 5 C intervals from Topt to 30 C (Staehr and

tank before measurements under selected temperatures: 5, 10, 15, Wernberg, 2009).

◦

20, 25 and 30 C, representative of the range of temperatures nor- Two-way analysis of variance (ANOVA) was used to test the

mally experienced by kelps in this region during an annual cycle effects of increasing temperatures on the functional variables and

◦

(Tuya et al., 2012) and two extremes: 5 and 30 C. Pre-cooled, or pre- estimates (GPmax, Rd, Q10 and reduction of Q10). Temperature (six

◦

warmed, water was used for each incubation; all incubations were levels: 5, 10, 15, 20, 25, 30 C) and the group case (intertidal

done using ﬁltered sea water (1 and 5 ␮m) to avoid the inﬂuence L. ochroleuca, inter- and subtidal S. polyschides) were treated as

of phytoplankton photosynthesis on ﬁnal results and 3 individual crossed, ﬁxed factors. Some of the data did not conform to the

plants – replicates – were used for incubations for each species and assumptions of ANOVA; the signiﬁcance of results were inter-

temperature. Changes in O2 concentrations were measured con- preted according to Underwood (1997), i.e. when data violated the

tinuously using a multi HQ40D (Hach Lange®) oxygen probe for assumption of homogeneous variances, the signiﬁcance was set at

each incubation, which had a duration of ∼20 min. After the incu- the ˛ = 0.01 level to decrease a type I error rate. Tukey’s tests were

◦

bations, seaweeds were oven-dried at 45 C for 48 h and the dry used as pairwise comparisons to resolve differences among levels

weight recorded. All data from the oxygen probes was corrected of signiﬁcant factors. Statistical analyses were performed using the

with the algal dry weight (DW) and the volume of the incubation STATISTICA 8 software package (Stat Soft. Inc., 2007).

tank to express all functional response variables per g DW of algae

−1 −1

l h (Staehr and Wernberg, 2009). To be able to discard possible

procedural artifacts we performed additional blind incubations to 3. Results

examine respiration/production rates in the ﬁltered seawater used

in our incubations and found negligible values. Gross primary productivity gradually rose until the optimum

◦

The maximum rate of gross productivity (GPmax) was calculated temperatures, i.e. around 16 C for L. ochroleuca and S. polyschides

◦

by adding the absolute value of respiration (Rd) to values recorded from the intertidal and 10 C for subtidal S. polyschides (Table 1),

for net primary productivity from all light intensities. Three addi- above which the rate of photosynthesis decreased (Fig. 1). For

tional parameters were determined by non-linear regression of both kelp species from the intertidal, optimum temperature was

gross photosynthesis (GPP) normalized by dry weight (DW) and determined through the piecewise regression model. For subtidal

irradiance (E), according to the model of Eilers and Peeters (1993): S. polyschides, the breakpoint was based on mean of GPmax val-

ues (Fig. 1C). For dark respiration, no optimum temperature was

◦

observed, as the rate of Rd was steadily rising until 30 C (Fig. 2).

GPmax2(1 + ˇ)(E/Iopt) −1 −1

GPmax reached ca. 8, 18 and 15 mg O g DW h for intertidal GPP = (1) 2

E/I

( opt) + 2ˇE/Iopt + 1 L. ochroleuca, and inter- and subtidal S. polyschides, respectively

(Fig. 1). These values were signiﬁcantly different between inter-

where GPmax is the maximum productivity at selected irradiance tidal L. ochroleuca and inter- and subtidal S. polyschides (two-way

and temperature, Iopt is the optimum light intensity and, in case ANOVA, Table 2), with a signiﬁcant higher value for intertidal S.

of photo-inhibition due to excess of light, the slope of photo- polyschides than L. ochroleuca (Tukey’s post hoc test, p < 0.001). The

inhibition ( ) was also determined (modeled with the R v2.15.0 difference in productivity between inter- and subtidal S. polyschides

open software, The R Foundation for Statistical Computing 2012). was not so pronounced, but still statistically signiﬁcant (Tukey’s

Furthermore, the light saturated gross productivity (GPmax) post hoc test, p < 0.001).

dependency on temperature was plotted through piecewise regres- Experimental temperatures signiﬁcantly affected the rates of

sion (‘segmented’ package, R v2.15.0). This model determines the respiration (two-way ANOVA, Table 2, Fig. 2), with intertidal S.

‘breakpoint’ of the regression, which is the optimum temperature polyschides having the strongest increase. Additionally, post hoc

(Topt) for photosynthesis, and its initial slope (Muggeo, 2008). How- Tukey’s tests showed signiﬁcantly higher values for intertidal S.

ever, algorithms used by the piecewise model were exclusively polyschides than L. ochroleuca (p < 0.001) and for subtidal than inter-

applied to kelps from the intertidal, as the model was not able tidal S. polyschides (p < 0.029).

to detect the ‘breakpoint’ for subtidal S. polyschides, due to the Q10 values for both NPP and GPP differed between cases

restrictions on the ﬂat relationship determination of the algorithm (two-way ANOVA, Table 2); the highest value was recorded for

(Vito Muggeo, pers. com.). Therefore, Topt for subtidal S. polyschides subtidal S. polyschides, which was signiﬁcantly different from

was based on mean values of gross primary production along the both kelp species from the intertidal (Tukey’s post hoc, p < 0.001,

increasing temperature, where the highest value was chosen as the Tables 1 and 2). In the intertidal, Q10 tended to be, although not

optimum temperature. statistically signiﬁcant, higher for L. ochroleuca than S. polyschides

Differences in the temperature responses of GPP and NPP below (Tables 1 and 2). The values of reduced Q10 estimates (calcu-

◦

the optimum temperature were assessed with Q10 values, which lated for temperatures above Topt to 30 C) showed a signiﬁcant

were calculated as: decrease in metabolic rates for all cases under increasing tempera-

/ T −T tures (two-way ANOVA, Table 2). Importantly, L. ochroleuca showed

rate2 [10 ( 2 1)]

Q = (2) the strongest drop in metabolism above the optimum temperature

10 rate1

(Table 1), which was signiﬁcantly larger than subtidal S. polyschides

120 S. Biskup et al. / Aquatic Botany 113 (2014) 117–122

Table 1

Estimates from ﬁtted temperature-response curves for gross (GPP) and net (NPP) photosynthesis and respiration (Rd) of intertidal L. ochroleuca and inter- and subtidal S.

◦ ◦

polyschides. Topt ( C) is the temperature at which maximum rates were found. Q10 is the relative change in metabolism with a 5 C increase in experimental temperatures.

◦

Reduction of Q10 above Topt is the relative decrease of metabolism from Topt to 30 C (mean ± SE, na – not applicable).

Topt Q10 Reduction of Q10 above Topt

NPP

Intertidal L. ochroleuca 16.090 ± 2.239 2.484 ± 0.948 1.149 ± 0.576

± ±

Intertidal S. polyschides 16.410 2.500 2.597 1.078 0.936 ± 0.031

Subtidal S. polyschides 10.000 2.587 6.546 ± 0.000 0.812 ± 0.119

Intertidal L. ochroleuca na 10.292 ± 7.685 Na

Intertidal S. polyschides na 5.758 ± 4.988 Na

Subtidal S. polyschides na 3.693 ± 0.000 Na

GPP

± ± ±

Intertidal L. ochroleuca 15.000 3.190 2.563 0.781 1.141 0.536

Intertidal S. polyschides 16.070 ± 2.893 2.682 ± 1.212 1.000 ± 0.011

Subtidal S. polyschides 10.000 ± 2.587 6.379 ± 0.000 0.898 ± 0.121

a (Tukey’s post hoc, p < 0.0025), and larger, although not statistically

22 signiﬁcant, than intertidal S. polyschides.

18 4. Discussion

14 We hypothesized that Portuguese native kelp species would

show an increase in functional responses with increasing tem-

peratures and our results supported our expectations. We tested

the consistency of these physiological responses to temperature

between juvenile sporophytes of L. ochroleuca and S. polyschides

from the intertidal. Our results showed that, due to their different

reproductive strategies, the functional responses to temperature

vary, including rates of productivity at optimum temperatures.

Moreover, this study showed that there is signiﬁcant variability in

b the functional response of S. polyschides when exposed to increas-

ing temperature between individuals from the inter- and subtidal.

The optimal temperature for productivity for intertidal L.

◦ ◦

18 ochroleuca and S. polyschides was around 16 C and 10 C for subti-

dal S. polyschides. Similar values were reported by Izquierdo et al.

14 (2002), where optimum temperatures for L. ochroleuca ranged

◦ ◦

from 15 C to 18 C. In this study, we observed a signiﬁcant dif-

max

10 ference between optimum temperatures for inter- and subtidal S.

polyschides. This supports the notion of the highly adaptable capac-

ity of this species to environmental conditions. Plastic responses,

expressed as physiological variations to changing environmental

conditions, are key mechanisms for macroalgae to occupy a broad 2

Table 2

c Two-way ANOVA testing the effect of temperature and group case (intertidal L.

ochroleuca, inter- and subtidal S. polyschides) on GPmax, Rd, Q10 and reduced Q10.

Effects that were found signiﬁcant are in bold, ns–not signiﬁcant (at p > 0.05). C

Source df MS F p

14 max

Temperature 5 58.303 11.062 <0.001

Group 2 332.868 63.156 <0.001

10 Temp × Group 10 23.098 4.383 <0.001

Residual 36 5.271

Temperature 5 5.514 39.077 <0.001

Group 2 2.032 14.404 <0.001

Temp × Group 10 0.344 2.441 <0.05

Residual 36 0.141

Q10

0 5 10 15 20 25 30 35 Temperature 5 0.000 0.000 ns

o Group 2 77.214 16.797 <0.001

Temperature ( C) Temp × Group 10 0.000 0.000 ns

Residual 36 4.597

Reduction of Q10

Fig. 1. Temperatures dependency of photosynthesis for (a) intertidal L. ochroleuca,

Temperature 5 0.000 0.000 ns

(b) intertidal S. polyschides and (c) subtidal S. polyschides. GPmax is in

− −

1 1 Group 2 0.564 6.932 <0.01

mg O2 g DW h . For detailed optimum temperature (Topt) determined by the

Temp × Group 10 0.000 0.000 ns

model/calculations see Table 1.

Residual 36 0.081

S. Biskup et al. / Aquatic Botany 113 (2014) 117–122 121

a sporogenesis only after the second year (Birkett et al., 1998;

3.5

Bartsch et al., 2008). Pereira et al. (2011) compared the ability of L.

ochroleuca and S. polyschides to recover after disturbances, empha-

sizing the pioneer and opportunistic nature of the latter due to its

2.5

annual life cycle.

The sensitivity of kelps’ metabolism to temperatures below and

above T was modeled through the Q parameter. Subtidal S.

1.5 opt 10

polyschides showed higher values than intertidal individuals, indi-

cating its faster onset of primary production. This ﬁnding suggests

0.5 that subtidal S. polyschides would be more sensitive to tempera-

ture changes. Compared to the intertidal, the subtidal is relatively

more stable in terms of potential sources of stress and disturb-

-0.5 ance, including temperature ﬂuctuations (e.g. Moran, 1999). This

would explain a lower acclimation capacity of S. polyschides from

the subtidal to environmental ﬂuctuations, compared to inter-

3.5 b

tidal specimens. Intertidal S. polyschides showed a trend for higher

metabolic rates under low (i.e. below the optimum) temperatures

than L. ochroleuca, but these did not exceed those observed for sub-

2.5

tidal S. polyschides. This further supports the idea that intertidal

specimens are more adapted than those from the subtidal to envi-

1.5 ronmental changes (Somero, 2002), and that differences between

the two intertidal kelps may be mostly driven by species-speciﬁc

Respiration

reproductive strategies (Pereira et al., 2011).

0.5 The response of macroalgae to supra-optimal temperature was

also tested and expressed as a reduction of Q10 values above the Topt.

The strongest decrease in both gross (GPP) and net (NPP) primary

-0.5

productivity was recorded for L. ochroleuca, in agreement with pre-

vious ﬁndings documenting up to four times higher mortality rates

due to higher temperatures for L. ochroleuca than S. polyschides

3.5 c

(Pereira et al., 2011). This physiological limitation of L. ochroleuca

(Roleda et al., 2004) and its restricted capability to acclimatize

to high temperatures (Bolton and Lüning, 1982; Izquierdo et al.,

2.5

2002) could have a reﬂection on its distribution. Further south from

the sampling location, populations of L. ochroleuca occur mainly at

1.5 depths below 40 m (Tittley et al., 2005), as the upper parts of the

shore might be exposed periodically to high temperatures (Van den

Hoek, 1982; Pereira et al., 2011) or in areas associated with intense

0.5 upwelling (Fernández, 2011). In contrast, across the same latitudes,

S. polyschides is capable of growing almost until the surface, and

so subjected to higher temperature ﬂuctuations (Van den Hoek,

-0.5

1982). In the future, under predicted scenarios of ocean warming,

this might lead to a change in the distribution range of L. ochroleuca

0 5 10 15 20 25 30 35 (northward retreat) and\or limit the existing populations to deeper

o habitats (Roleda et al., 2004).

Temp erature ( C)

In summary, we have demonstrated that distinct kelp species

inhabiting the same geographical area may have different func-

Fig. 2. Temperature-dependency of dark respiration for (a) intertidal L.

2 tional responses to increasing temperatures, and so they will not

ochroleuca (y = 0.048x − 0.057, R = 0.659, p-value = 0.050), (b) intertidal S.

2 be equally affected by predicted ocean warming. In particular,

polyschides (y = 0.066x + 0.169, R = 0.736, p-value = 0.029) and (c) subtidal S.

polyschides (y = 0.067x − 0.291, R = 0.809, p-value = 0.015). Dark respiration is in L. ochroleuca has a more limited physiological plasticity than S.

−1 −1

mg O2 g DW h . polyschides, and might therefore be more susceptible to the effects

of ocean warning.

range of physical environments (Sultan, 2001). Phenotypic plastic-

ity was previously reported for other kelp species, such as Laminaria Acknowledgements

digitata (Delebecq et al., 2012) and Ecklonia radiata (Wing et al.,

2007). Physiological plasticity was noted for the kelp E. radiata This work is part of a Master thesis by S. Biskup, within

(Staehr and Wernberg, 2009) through acclimation of photosynthe- the Erasmus Mundus Course in Marine Biodiversity and Conser-

sis and respiration rates to increasing ocean temperature. vation (EMBC). Pedro Duarte, Manuela Ramos and Luis Magina

Metabolic rates (GPmax and Rd) of intertidal S. polyschides were helped during ﬁeld work. Mario Leitão and “Cavaleiros do Mar”

higher than L. ochroleuca; these ﬁndings likely reﬂect the different provided technical assistance and boat facilities during diving.

life spans of these kelps. Annual S. polyschides must develop all life Fabio Rindi and Vito Muggeo provided valuable suggestions on

stages, including sporophyte growth, gametophyte formation and taxonomy and physiology of kelps. This research was supported

reproduction, within several months. In spring, fast growth pre- by the projects PHYSIOGRAPHY (PTDC/MAR/105147/2008) and

pares kelps for maturation and sporogenesis, followed by decay OCEANKELP (PTDC/MAR/109954/2009), funded by the Portuguese

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nual L. ochroleuca does not require such intensive pace, as it starts the European Regional Development Fund (ERDF) through the

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