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Temperature-dependent photosynthesis in the intertidal algaFucus

gardneriand sensitivity to ongoing climate change

Nicholas B. Colvard a,, Emily Carrington b, Brian Helmuth a

a Marine Science Center, Northeastern University, Nahant, MA 01908, USAb Department of Biology and Friday Harbor Laboraties, University of Washington, Friday Harbor, WA, 98250, USA

a b s t r a c ta r t i c l e i n f o

Article history:

Received 10 February 2014Received in revised form 29 April 2014

Accepted 1 May 2014

Available online 21 May 2014

Keywords:

Climate change

Fucus gardneri

Intertidal

Photosynthesis

Tidal cycle

Understanding the photosynthetic responses of marine macroalgae to changes in their thermal environment is

vital to characterizing the success of these habitat-forming primary producers in the face of climate change.We measured net photosynthesis in apical tips ofFucus gardnericollected from the intertidal zone of Friday

Harbor, WA over a range of irradiancelevels(01500 mol photons m2 s1) at 10,14,and 18 Cto determine

levels of saturating irradiance. We then recorded net photosynthesis at saturating irradiance in tips exposed to

seawater temperatures ranging from 6 to 22 C, as well as dark respiration. Results show that F. gardneriat

this location has a peak in net photosynthesis at 1618 C seawater temperature, with signicant declines in

net photosynthesis at 20 and 22 C. Respiration showed a positive linear relationship with increasing seawater

temperature. Using archived seawater temperature, irradiance, and tidal data, we produced a model of net pho-

tosynthesis over two years (October 2010October 2012). Maximal seawater temperatures recorded at FHL

rarely exceeded 14 C, suggesting that an increase of +2 and +4 C in seawater temperature would lead to

increased net photosynthesis at this site. These results allowed us to develop a predictive model to forecast the

net photosynthesis ofF. gardneriat different intertidal elevations to explore the effects of seawater temperature

andirradiance on netphotosynthesis.We alsoexaminedthe effects of thetimingof hightide,testing thehypoth-

esis thatnet photosynthesis will be highest at sites where submersion occursduring peak levelsof irradiance. Our

results suggest that as seawater temperatures increase (up to +4 C above ambient) F. gardneribelow +1 m

MLLW tidal elevation will experienceincreasesin net photosynthesis. These analyses also suggest thatthe effectsof environmental change may depend in part on tidal regime, which determines the extent to which algae are

submerged during times of day when irradiance is high.

2014 Elsevier B.V. All rights reserved.

1. Introduction

A fundamental goal of global climate change research is to under-

stand how organisms will likely respond physiologically to novel envi-

ronmental conditions (Chown and Gaston, 1999; Somero, 2002) and

how the inuence of climatic factors may be modied by other non-

climatic factors (e.g.,Mislan et al., 2011). Intertidal and shallow subtidal

organisms have long served as model systems for examining the im-

pacts of the physical environment on patterns of distribution in nature

(Paine, 1994). To this end, many studies have examined the effects of

lethal temperatures in setting the local and geographic distribution

of intertidal and shallow subtidal organisms (Wethey et al., 2011). A

number of recent studies have emphasized the importance of also

considering the sublethal effects of environmental change on marine

animals (Howard et al., 2013), for example theinuence of temperature

on rates of foraging (Kordas et al., 2011; Sanford, 2002), growth

(Almada-Villela et al., 1982), and reproduction (Petes et al., 2008).

Comparable studies of macroalgae have been conducted examining

the effects of temperature and desiccation on rates of survival, photo-

synthesis, and growth (Bell, 1993; Matta and Chapman, 1995; Zou

et al., 2007). A principal consideration is the importance of local factors,

often non-climatic in nature, in modifying the inuence of environmen-

tal factors related to climate change. For example, wave exposure and

the timing of low tide can signicantly affect the risk of thermal stress

in intertidal organisms (Mislan et al., 2011), and the vulnerability of

invertebrates to thermal stress can be signicantly affected by food

supply and the presence of other stressors, such as pollution (Howard

et al., 2013).

Several studies have shown that, for some populations, small

increases in temperature may lead to increases in performance,

especially at a species' poleward distributional limits or to decreases at

their equatorial limits (Howard et al., 2013; Somero, 2002). Other stud-

ies have suggested that prolonged exposure to sublethal conditions can

lead to large-scale mortality due to the cumulative effects of environ-

mental stress on energetics (Woodin et al., 2013). Surprisingly, how-

ever, while lethal thermal limits have been relatively well studied for

many species, complete thermal performance curves describing the

Journal of Experimental Marine Biology and Ecology 458 (2014) 612

Corresponding author. Tel.: +1 781 581 7370x331; fax: +1 781 581 6076.

E-mail address:[email protected](N.B. Colvard).

http://dx.doi.org/10.1016/j.jembe.2014.05.001

0022-0981/ 2014 Elsevier B.V. All rights reserved.

Contents lists available at ScienceDirect

Journal of Experimental Marine Biology and Ecology

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j e m b e
http://dx.doi.org/10.1016/j.jembe.2014.05.001http://dx.doi.org/10.1016/j.jembe.2014.05.001http://dx.doi.org/10.1016/j.jembe.2014.05.001mailto:[email protected]://dx.doi.org/10.1016/j.jembe.2014.05.001http://www.sciencedirect.com/science/journal/00220981http://www.sciencedirect.com/science/journal/00220981http://dx.doi.org/10.1016/j.jembe.2014.05.001mailto:[email protected]://dx.doi.org/10.1016/j.jembe.2014.05.001http://crossmark.crossref.org/dialog/?doi=10.1016/j.jembe.2014.05.001&domain=pdf


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effects of temperature on marine organism performance are compara-

tively rare (Monaco and Helmuth, 2011). In cases where we do have a

thorough knowledge of how populations are likely to respond to tem-

perature, studies have shown that local adaptation (Kuo and Sanford,

2009) and low genetic diversity (Pearson et al., 2010) can potentially

create large differences in thermal tolerance between populations and

among closely related species. This lack of information for many ecolog-

ically important species limits our ability to predict how changing

temperatures likely impact marine ecosystems.In this study we explore the effects of seawater temperature and

irradiance on a common, ecologically important species of marine

alga,Fucus gardneri.F. gardneriserves as a primary producer for the

mid-intertidal region, and thus as a food source for littorine snails,

isopods, and amphipods, and can produce large algal mats that serve

as protection for intertidal invertebrates (Dethier, 1982). Given this spe-

cies' foundational ecological role in the Northeastern Pacic intertidal

zone, an explicit understanding of how F. gardneriis likely to respond

to ongoingchange is paramount. It is well understood that temperature

and irradiance inuence photosynthesis in fucoids (Kraufvelin et al.,

2012; Nygard and Dring, 2008; Williams and Dethier, 2005 ). For

example,Dethier and Williams (2009)showed thatF. gardneriphoto-

synthesis, growth, and reproduction were most inuenced by seasonal

differences in environmental temperature and irradiance levels. Previous

studies of brown algae have documented the effects of irradiance levels

on photosynthetic capacity (Dring and Brown, 1982; Dromgoole, 1987,

1988; Johnson et al., 1998; Williams and Dethier, 2005), somatic growth

(Davison and Pearson, 1996; Dethier and Williams, 2009; Falkowski and

LaRoche, 1991; Kim et al., 2011; Kbler and Dudgeon, 1996; Lning,

1971), and reproductive development (Davison and Pearson, 1996;

Dethier and Williams, 2009). Several studies have also evaluated the

photosynthetic performance of macroalgae in relation to environmental

temperature (Bell, 1993; Kim et al., 2011; Kbler and Davison, 1993;

Matta and Chapman, 1995; Williams and Dethier, 2005), where many

have found an initial positive relationship between photosynthesis and

increases in seawater temperature above current eld conditions.

Research on Fucus vesiculosus (Alexandridis et al., 2012; Kraufvelin

et al., 2012; Middelboe et al., 2006; Nygard and Dring, 2008; Terry and

Moss, 1981) has demonstrated how light and temperature can inuencegermination, recruitment, growth, and photosynthesis in this alga.

Although previous research has evaluated the photosynthetic activity

ofthePacic species F. gardneri (previouslyF. distichus) to environmental

change (Johnson et al., 1974; Quadir et al., 1979; Williams and Dethier,

2005), these studies evaluated photosynthesis under a fairly narrow

temperature range (e.g., summer temperatures).

Our study expands upon previous work examiningF. gardneripho-

tosynthesis in order to characterize how this species will likely respond

to a range of seawater temperatures including those predicted in the

near future. As previously described for other algal species (Bell, 1993;

Dromgoole, 1988; Williams and Dethier, 2005), we hypothesized that

increased seawater temperature would generally increase net photo-

synthesis inF. gardneriup to some (previously unidentied) optimal

temperature, but beyond this thermal optimum productivity woulddecline (Davison and Pearson, 1996). We further quantied patterns

of seawater temperature in the intertidal zone at FHL to determine

how close environmental conditions at this site currently are relative

to this species' thermal optimum and how future increases in seawater

temperature will likely affectF. gardneripopulations. Finally, we evalu-

ated the potential role of the tidal regime in driving sensitivity to envi-

ronmental change. While it is well recognized that the timing of low

tide determines the frequency by which organisms are exposed at low

tide to extreme aerial conditions of temperature and desiccation during

the hottest parts of the day (Helmuth et al., 2002; Orton, 1929), a less

explored corollary for intertidal algae is that maximal levels of photo-

synthesis are likely to occur when high tides occur mid-day when

irradiance levels are highest. The primary goals of this research were

to (a) determine the photosynthetic performance curve for F. gardneri

with increasing temperature at a saturating irradiance and in the dark;

(b) develop a generic net photosynthesis model that can be used to pre-

dict net photosynthesis (Pnet) under a range of future temperature and

irradiance combinations at FHL; (c) to explore the relative importance

of thetiming of high tide in driving sensitivity to environmental change;

and (d) evaluate whether the current southern range limit ofF. gardneri

is likely to be set by temperature.

2. Materials and methods

2.1. Study location and algal collection

All algal specimens were collected from the mid-intertidal region

(~0.51 m above Mean Lower Low Water, MLLW) along the coastline

near FHL between May and August 2012. This tidal elevation harbors

denseFucusalgal mats as well as herbivorous grazing littorine snails,

isopods, and amphipods (Dethier, 1982; Dethier et al., 2005). All algal

specimens collected were free of grazers and epiphytes, and had mini-

mal tissue damage to the thallus or wingregions.

Seawater temperatures collected from October 2010October 2012

(http://depts.washington.edu/fhl/fhl_wx.html ) showed that seawater

temperature at FHL rarely drops below 7 C, and rarely exceeds 14 C

at 1.7 m depth (Fig. 1); though surface waters can exceed 14 C on

warm summer days. Future climate models suggest an average increase

in sea surface temperature of 2.3 C by the year 2090 for the North

Pacic region (IPCC, 2007). Maximal water temperatures near the

equatorial edge of this species' southern range (Monterey Bay, CA) are

approximately 17.4 C from 2010 to 2012 (www.ndbc.noaa.gov). We

therefore selected a temperature range of 6 to 22 C for our experi-

ments, to encompass temperatures experienced by this species over

much of its range, both now and in the near future.

AllF. gardneriwere maintained in a ow-through seawater table

where theywerekept for 2472 h before photosynthetic measurements

were conducted. Experiments were conducted on the apical tip, the

growing region, which was cut from a whole algal thallus 24 h prior

to photosynthesis measurements to avoid wounding response. At

the end of the experiment, the dry weights of all algal tissues were

Fig. 1.Frequency distribution of surface seawater temperatures from October 2010 to

October 2012 at Friday Harbor Laboratories, Washington (http://depts.washington.edu/

fhl/fhl_wx.html). The rst peak in the frequency of temperature (78.5 C) is largely

based on fall and winter-time measurements, whereas the second peak (9.510.5 C) is

primarily comprised of spring and summer time measurements. The inset gure is of

time-series data from which the frequency distribution was calculated, with hourly

seawater temperature measurements ranging from 6 to 16 C (y-axis) from October

2010 to October 2012 (x-axis).

7N.B. Colvard et al. / Journal of Experimental Marine Biology and Ecology 458 (2014) 612
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measured (dried to constant weight at 80 C) in order to standardize all

photosynthetic measurements.

2.2. Photosynthetic measurements of Fucus gardneri

Net photosynthesis of the apical tips (~ 2 cm2) of F. gardneri

was measured using a Hansatech DW3 chamber system (Hansatech,

Norfolk England) with a Clark-type oxygen electrode (Bell, 1993;

Maberly, 1992). This 10 mL closed volume chamber was temperature-controlled by a recirculating water jacket connected to a chiller, and

a 300-W quartz-halogen lamp projector was used as an external

light source and light levels were manipulated using neutral density

lters. All seawater used in the experiments was ltered through a

10-micron lter bag, and the seawater was replaced for each individual

alga measured.

A preliminary set of experiments was conducted to quantify the sat-

urating irradiance for F. gardneri apical tips by recording photosynthesis

as a function of irradiance (PI curves) at 10, 14, and 18 C 0.1 C.

These seawater temperatures are representative of ambient (recorded

temperature), high, and extreme (respectively) summer conditions at

FHL. The PI curves were generated using a range of irradiance levels

from 0 to 1500mol photons m2 s1. Specimens were dark acclimat-

ed for 1 h before respiration measurements. Apical tips (n = 3 per tem-

perature) were non-reproductive (0.021 0.005 g dry wt., n = 9) to

avoid tissue that did not contribute to photosynthesis (Fig. S1). Oxygen

production was calculated based on rate of change in O2, normalized by

dry oven weight of the algal tissue.

A curve was t to all points in each of the three PI curves using the

following equation (Jassby and Platt, 1976):

Pnet Pgross; max tanh I=Pgross; max

h iRd 1

where Pnetis net photosynthesis (mol O2g dry wt.1 h1), Pgross,max

is the maximum rate of gross photosynthesis at saturating irradi-

ance (mol O2g dry wt.1 h1), is the initial slope of the curve

([mol O2 g dry wt.1][mol photons m2]1), I is irradiance

(mol photons m2 s1), and Rdis the respiration rate in the dark(mol O2g dry wt.

1 h1). Pgross,maxwas calculated posthoc from

Pnet,max (the maximum rate of net photosynthesis at a saturating

irradiance [mol O2 g dry wt.1 h1]) and Rd, where Pgross,max =

Pnet,max + Rd. The saturation irradiance (Ik) was determined by

Pgross,max/. These parameters allowed us to further test the photo-

synthetic performance ofF. gardneri conditioned with a range of

temperatures.

2.3. Effect of seawater temperature on photosynthesis

We measured net photosynthesis ofF. gardneri under saturating

irradiance at 2 C intervals between 6 and 22 C. Based on the results

of the preliminary PI curves (above), which showed no signicant

difference in saturating irradiance (Ik) among the three temperaturestested, we used an irradiance of 1400 mol photons m2 s1 for all

Pgross,max measurements, as this level was reliably above minimum satu-

rating irradiance for all temperatures. For the dark respiration measure-

ments, allalgal tissuewas dark-adapted forat least 1 h. We measured 10

replicate apical tips ofF. gardnerifor each temperature evaluated.

2.4. Net photosynthesis model

Using parameters from our net photosynthesis measurements

in conjunction with varying irradiance (I, 01500 mol photons

m2 s1) and water temperature (622 C) combinations, we devel-

oped a simple model to predict net photosynthesis (Pnet). This predic-

tive model is based on best curve ts for Pgross,max (second order

polynomial curve t) and Rd(a linear equation); both parameters are

dependent on seawater temperature. However, there were no differ-

ences in initial slope of the PI curve () between temperatures, there-

fore a xed value was used for all conditions. The Pnetmodel, which is

dependent only on water temperature and irradiance, is valid only for

submersed conditions, and we are assuming that Pnet 0 during aerial

exposure, since the mean net photosynthesis for F. gardnerihas been

shown to be as much as two orders of magnitude lower in air than in

water (Williams and Dethier, 2005).

We thenusedthismodel to reconstruct Pnet based on environmentalconditions recorded at FHL over two years (October 2010October

2012) (http://depts.washington.edu/fhl/fhl_wx.html). Seawater tem-

perature was measured in situ and underwater downwelling irradiance

was estimated from surface irradiance and water depth following Beer's

Law:

Id;uw z IaireKdz

2

where Id,uwis the downwelling underwater irradiance (mol photons

m2 s1) atdepthz (in meters),Iair is the downwelling irradiance mea-

sured inair(mol photons m2 s1), Kd is the vertical light attenuation

coefcient for summer (0.373 m1, based onDethier and Williams,

2009). Tidal predictions were used to estimate water depth (z) at an

intertidal elevation of + 1 m MLLW (Xtide,http://tbone.geol.sc.edu/

tide). Thus, when the predicted tidal level was b+1 m MLLW, then

the alga was assumed to be aerially exposed and Pnet= 0.

To evaluate the impact an increase in seawater temperature would

have on Pnetover the tidal range ofF. gardneri, we calculated the yearly

average Pnetfor FHL from hourly recorded data, and compared it to

simulated increases in temperature +2 C and +4 C above recorded

temperatures at intertidal elevations ranging from 1.0 m to +2.5 m

MLLW, at 0.1 m intervals. Using only recorded temperature conditions

at FHL, we then manipulated the timing of the tide to quantify yearly

average Pnet, shifting the tidal timing at FHL by 6 h, 3 h, +3 h,

and + 6 h from ambient (+ 0 h difference). We then evaluated the dif-

ference in yearlyaverage Pnet atthe ve tidal adjustments using thetidal

cycle at Tatoosh Island, WA. Tatoosh Island is located ~190 km west of

FHL, typically exhibiting a 35 h difference in tidal timing ahead of

FHL (Xtide). Preliminary results suggested that the greatest differencein yearly average Pnetwas between +0 m and 0.5 m MLLW intertidal

elevation, therefore we used these two elevations to explore the effects

of exposure and submersion time on yearly average Pnet.

In order to evaluate the likelihood that the southern latitudinal

range limit ofF. gardneriwas set by seawater temperature conditions,

we compared the yearly average Pnet using temperatures recorded

during 20102012 at FHL, as well as at Monterey, CA, the recorded

southern limit ofF. gardneri(Blanchette et al., 2008), and at San Diego,

CA, considerably farther south than the current range limit. We also

estimated Pnet at each of these sites using temperature increases

of 2 C and 4 C above current conditions. Seawater temperature data

for the three sites were obtained from NOAA Buoy Center (www.ndbc.

noaa.gov). We recognize that this analysis is based only on seawater

temperatures, and thus ignores all other environmental conditionslikely to change over this range. The analysis also does not consider

any potential physiological differences among populations. However,

we made the assumption that if any differences do exist, populations

farther south are likely to be even more thermally tolerant than those

at FHL. Our comparison thus provides a conservative estimate of yearly

average Pnetfor F. gardnerialong the northeastern Pacic, and actual

values could be higher at southern sites if algae were acclimatized or

adapted to those conditions.

A linear regression was used to determine the relationship between

algal respiration and temperature. A two-factor mixed model ANOVA

wasused to compare yearly average Pnet at FHL at current temperatures

and increasesof 2 C and 4 C with changes in tidal elevation. Sensitivity

analyses were used to evaluate differences in yearly average P netbe-

tween FHL and Tatoosh Island, and compare yearly average Pnetwith

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response to temperature differences between latitudinal sites (Friday

Harbor, WA, Monterey, CA, and San Diego, CA). All statistical tests

were run with Systat 12.

3. Results

3.1. Effect of seawater temperature on photosynthesis

Best curve

ts were applied to the photosynthetic performancemeasurements ofF. gardneriin response to changes in temperature in

the dark (Rd) and at a saturating irradiance (Pgross,max) (Fig. 2). A linear

regression analysis showed a signicant increase in respiration, Rd, with

temperature (r2 = 0.798, P b 0.001) from 34.70 2.41 mol CO2g dry wt.1 h1 at 6 C up to 49.33 3.17 mol CO2g dry wt.

1 h1

at 22 C. A non-linear regression (second order polynomial) curve was

t to the photosynthesis data to describe the effect of temperature on

Pgross,max, and showed a maximum value of 16 C, followed by a de-

crease in Pgross,maxfrom 18 to 22 C (Fig. 2). Temperature had a small

effect on the light-saturated, maximum rate of photosynthesis of sub-

mergedF. gardneri, with Q10values of 1.52 at 616 C, 1.59 at 818 C,

and 1.15at 1020 C, demonstrating the greatest rate of change in pho-

tosynthesis associated to temperature changefor the818C range,and

quickly declining for the 1020 C range.

3.2. Net photosynthesis model

The predictive model of PnetforF. gardneribased on the measured

seawater temperature and downwelling irradiance calculated from

aerial measurements at FHL (shown as points overlaid on the contour

plot, Fig. 3), suggest that submerged F. gardneri at FHL never experienced

temperatures above optimal levels. The two-factor mixed model ANOVA

showed a signicant difference in net photosynthesis for F. gardneri

when evaluating the interaction of tidal elevation temperature change

(F2,102 = 3.939, P = 0.022) (Fig. S2). As expected, simulations show that

photosynthesis decreases with increased tidal elevation, especially N +

1 m MLLW.

The Pnet model simulations for different adjustments to the timingof

the tide for FHL showed the greatest increase in Pnetwith shifts in tidal

timing of6 h and +6 h (Fig. S3). Using tide predictions for Tatoosh

Fig. 2. Maximum gross photosynthesis (Pgross, max-closed circles) and dark respiration

(Rd-open circles) for apical tips ofFucus gardneriin seawater. Symbols are means

SE of n = 10 replicates per temperature. A linear regression analysis showed there

was a signicant increase (r2 = 0.798, P b 0.001) in Rd(mol CO2g dry wt1 h1)

increasing with temperature, from 6 to 22 C. For Pgross,max(mol O2g dry wt1 h1),

the photosynthetic output increases with temperature up to 18 C, after which Pgross,max

shows a decline at 20 and 22 C.

Fig. 3. Contour plot of thepredictivemodelof Pnet for Fucus gardneri (mol O2 g dry wt.1

h1) for a range ofirradiance(01500 mol photons m2 s1) and seawater temperature

(6

22 C) combinations. The overlaid points are environmental databased on temperatureand underwater irradiance measurements from October 2010 to October 2012 at Friday

Harbor Laboratories, WA.

Fig. 4.The Pnetmodel simulations using ambient temperature conditions, evaluating the

difference in tidal timing for 0 m tidal elevation (A) and 0.5 m tide tidal elevation (B) for

Friday Harbor Laboratories (black bars) and Tatoosh Island (white bars). The yearly average

Pnet forthe ve tidal timing shifts (6 h to+6 h)showed the lowestPnet at0 h tidal timing

for FHL,but was lowest at+3 h forTatooshIslandat 0 m and 0.5m tidalelevation ofthealga.

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Island, only 6 h and 3 h tidal timing shift predicted an increase in

yearly average Pnetfor all intertidal elevations. However, a tidal timing

shift of +6 h caused a decrease in Pnet at tidal elevations b+1 m

MLLW, but an increase in Pnet at tidal elevations N+1 m MLLW

(Fig. S3). Theyearlyaverage Pnet for shifts in tidal timings demonstrated

the lowest Pnetat 0 h tidal timing for FHL at 0 m and 0.5 m tidal eleva-

tion, however for Tatoosh Island, yearly average Pnet was lowest at

+3 h for both tidal elevations (Fig. 4).

The model simulations evaluating yearly average Pnetfor currentrecorded temperatures (+0 C), and increases of 2 C and 4 C for San

Diego, CA, Monterey, CA, and Friday Harbor, WA revealed differences

in sensitivity to temperature increases between the three locations,

but more importantly show that the current southern limits is likely

not set by thermal performance (Fig. 5). Modeled Pnetfor San Diego,

CA temperatures showed positive yearly average Pnet, even though

this location is further south than the southern range limit for this

species (Blanchette et al., 2008). However, the model predictions for

this location suggest a decline in Pnet with increased seawater tempera-

ture, assuming that thermal sensitivity is comparable to algae from the

northern site. In contrast, there is no difference in yearlyaverage Pnet for

F. gardneribased on current and projected temperatures for Monterey,

CA. Andnally, yearly average Pnetat FHL is predicted to increase with

increasing seawater temperature (Fig. 5).

4. Discussion

This study demonstrated that the photosynthetic response of

F. gardneri is strongly dependent on surrounding seawater temperature

at high levelsof irradiance, andthat at most sites an increase in seawater

temperature will either have no effect on performance, or will slightly

increase photosynthetic performance. Whereas previous studies have

explored the plasticity of fucoids to wave action (Blanchette et al.,

2000; Dethier and Williams, 2009), desiccation (Dethier and Williams,2009; Gylle et al., 2009; Harker et al., 1999), and habitat type

(Chapman, 1995; Schonbeck and Norton, 1978, 1980; Wernberg et al.,

2011), this study is one of the rst to characterize the net photosynthe-

sis ofF. gardneriunder a range of irradiance and temperature combina-

tions in submerged conditions (but seeAlexandridis et al., 2012).

Our results show that 1618 C is the optimal temperature for

F. gardneri in submerged conditions at Friday Harbor, suggesting a

strong link between the organism's tness and the thermal envi-

ronment (Prtner, 2010) while undergoing maximum rates of gross

photosynthesis. The initial positive effect of temperature (b16 C) is

attributed to the role of temperature in carbon xation during photo-

synthesis up to a thermal maximum (Davison, 1991). This increase in

photosynthetic activity to increasing temperature is quantied by a

Q10value, which for F. gardnerihas been shown to vary between 1.1

Fig. 5.Fucus gardneriyearly average Pnetmodel predictions for current recorded temperatures (+ 0 C), and increases of 2 C and 4 C for Friday Harbor, WA (insert A), Monterey, CA

(insertB), andSan Diego, CA (insert C).The dashed line(near Monterey,CA) is thecurrentlyrecorded southernlimitofF. gardneri (Blanchette et al.,2008). These data show yearly average

Pnetis predicted to increase with increasing seawater temperature for Friday Harbor, WA, not differ in yearly average Pnetfor Monterey, CA, and decline in P netwith increased seawater

temperature in San Diego, CA. However, San Diego, CA is modeled to have positive net photosynthesis, though this location is further south than the southern limit ofFucusalgae in

the northeastern Pacic.

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and 1.5 (Madsen and Maberly, 1990, present study), for temperatures

between 6 and 20 C. Reduction in gross photosynthesis at tem-

peratures above 18 C can be attributed to several factors such as tem-

perature sensitive enzymes of photophosphorylation and electron

transport and plastoquinone diffusion (Davison, 1991). Oxygen-

dependent thermal tolerancecould also explain the near linear increase

in respiration with increasing temperature observed in submerged

conditions (Allakhverdiev et al., 2008; Zou et al., 2007). However, our

results should be interpreted with caution because they were conduct-ed on individuals from one location; there was a low power of compar-

ison among thePI curves (n = 3 per temperature), and becausethe net

photosynthesis model is based on the algal tissue from the apical tip

rather than the entire thalli. Moreover, experiments measuring temper-

ature effects were conducted at saturating irradiance, and modeled at

lower irradiance levels using a generic PI curve. Thus, explicit tests at

lower irradiance levelsare still needed. Additionally, we did not account

for the effect of ultraviolet radiation (UVR) onFucusphotosynthetic

activity over the range of temperatures evaluated;however, we suggest

that in situ UVR may also affect macroalgal net photosynthesis, primar-

ily during shallow submerged conditions and aerial exposure (Raven

and Hurd, 2012).

The optimum temperature of 16 C is ~2 C warmer than thehighest

recorded seawater temperature at FHLfrom 2010 to 2012. This suggests

thatF. gardnerimay be able to withstand the projected average sea-

water temperature increase of 2.3 C by the year 2090 for the North

Pacic region. Notably, however, this increase is based on changes in

average conditions only and it is highly likely that temperatures in

excess of the optimum will occur during rare, extreme events such as

those recorded in other parts of the world. For example, in summer

2012 temperatures in the Gulf of Maine were up to 3 C higher than

the 19822011 climatology (Mills et al., 2013).Somero (2010)sug-

gestedthat with projectedfutureclimate changeand organism acclima-

tization to increasing temperature, there will be winners and losers in

the intertidal; thendings from this study suggest F. gardneri at FHL will

likely increase net photosynthesis with increasing seawater tempera-

tures. These simulations predict that F. gardneriat low tidal elevations

(b+1 m MLLW) will experience an approximately10% increase in year-

ly average photosynthesis with a 4 C increase in seawater temperatureabove ambient.

The comparison of the Pnetmodels for F. gardneri based on tidal

timing suggests that the timing of high tide can theoretically inuence

yearly net photosynthesis by as much as 25% (Fig. 4). The tidal timing

and submergence time can inuence photosynthesis by determining

algal submergence during midday irradiance exposure, though this is

dependent on tidal elevation ofFucusalgae. The tidal regimes of FHL

and Tatoosh Island demonstrate that the timing of the tide, tidal

range,and duration of exposure time between these twolocationsinu-

ences yearly average PnetofF. gardneri; however, these effects are likely

to be compounded with differences in irradiance and water tempera-

ture between the two sites. The Pnetmodel simulations showed FHL

tidal timing manipulations caused the greatest change in net photosyn-

thesis when shifting the tide 6 h and +6 h from current conditions(i.e., ambient), though Tatoosh Island demonstrated an increase in net

photosynthesis when shifting the tide 6 h and 3 h from ambient.

Because simulations for Tatoosh Island used the same environmental

temperature and irradiance conditions measured at FHL, differences

observed in the yearly average Pnetare only attributable to differences

in tidal timing and range for these two locations, and do not include

the effects of differences in other environmental conditions(e.g., irradi-

ance, water temperature).

The Pnetmodel comparison for temperature data from San Diego,

CA, Monterey, CA, and Friday Harbor, WA suggests that F. gardneri

has a positive net photosynthesis at all three locations, though

Monterey, CA has been identied as the approximate southern

limit of this species. This suggests the southern limit for F. gardneri

is not solely temperature dependent, and is potentially limited by

other environmental conditions (i.e., spatial competition, foraging

pressure), or by some combination of stressors. However, macroalgae

at the more southern sites are expected to display a reduced photosyn-

theticresponse with increasingtemperature conditions,whereas Friday

Harbor shows a continued increase in photosynthesis with an increase

of 2 and 4 C in seawater temperature.

Future applications of this Pnet model should incorporate aerial

exposure and other abiotic conditions and biotic interactions that are

drivingFucus

tness in the intertidal zone. Duration of aerial exposureand environmental conditions duringexposure can dictate algal success

and net photosynthesis (Williams and Dethier, 2005).In our simplePnetmodel we suspended photosynthetic activity during aerial exposure

and did not account for potential deleterious effects of desiccation,

UVR, and heat stress during low tide events, especially during warm

summerdays. Other abiotic conditions thatmay inuence photosynthe-

sis along with temperature and irradiance are nutrient levels (Nygard

and Dring, 2008), salinity (Gylle et al., 2009; Nygard and Dring, 2008),

and CO2 concentrations (Zou and Gao, 2002). Future studies canexplore

the role these other environmental conditions may have on the Pnetof

F. gardneri.

This study is an initial step at describing the net photosynthesis of

F. gardneriusing a range of seawater temperatures, and therefore is a

critical rst step that can be expanded upon to explore how other envi-

ronmental factors (e.g., salinity, grazing pressure, water motion, and

aerial exposure) contribute to net photosynthesis in this intertidal alga.

Supplementary data to this article can be found online athttp://dx.

doi.org/10.1016/j.jembe.2014.05.001.

Acknowledgments

This work was supported by an Alan and Marian Kohn Fellowship

to NC from UW Friday Harbor Laboratories, as well as the US National

Science Foundation (NSF OCE_0926581 to BH and OCE_ 0824903

to EC) and National Aeronautics and Space Administration (NASA

NNX07AF20G to BH). We are grateful to M. Bracken and M. Zippay for

their comments on previous drafts of this manuscript. We would like

to thank two anonymous reviewersand editorial comments forimprov-ing this manuscript. We thank K. Sebens and the staff of the Friday

Harbor Laboratories for hosting our visit, as well as H. Hayford, O.

Moulton, and L. Newcomb for their support in the data collection. This

is publication number 314 of the Northeastern University Marine

Science Center.[SS]

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