TURNING UP THE HEAT

Intertidal environments are highly variable withrespect to temperature due to tidal cycles and thevertical elevation influencing the period of emer-sion, and thus rocky intertidal organisms generallyhave broad temperature tolerances. Many popula-tions of intertidal organisms, however, may alreadyexperience their physiological limits under current-day temperature profiles (Stillman and Somero2000, Nguyen et al. 2011). Such species are likely tobe highly sensitive to further increases in sea andair temperatures, increases in extreme temperatureevents, and changes to variability in temperature(Hawkins et al. 2008, Lima and Wethey 2012).

Increasing evidence (but see Poloczanska et al.2011) indicates that species range shifts are alreadyoccurring in response to increased sea-surface tem-perature with poleward expansions and contractionsat their equatorial limits (Millar 2007, Ling et al.2009b, Pitt et al. 2010, Johnson et al. 2011, Lastet al. 2011, Wernberg et al. 2011a). Amongstaffected species, macroalgae are particularly suscep-tible (Millar 2007, Johnson et al. 2011, Poloczanskaet al. 2011, Wernberg et al. 2011a) due to (1) thelack of potential reef habitat to retreat to on somecoastlines, (2) the apparently poor dispersal capacityof many macroalgae (Santelices 1990, Bellgroveet al. 2004, Coleman et al. 2009, 2011), and (3) theautogenic engineering role (Jones et al. 1994) ofmany vulnerable macroalgal species (Schiel 2006,Schiel 2011, Wernberg et al. 2011b). Elevated watertemperatures pose a significant threat to both mac-roalgae and their associated species of intertidaland shallow subtidal reefs (Schiel et al. 2004, Wern-berg et al. 2011a), with likelihood of local and glo-bal extinctions and the inevitable loss ofbiodiversity.

In this issue, Clark et al. “Potential for adaptationin response to thermal stress in an intertidal macro-alga” remind us that, although recent reviews havecalled for examination of the influence of genotypeon environmental tolerance (Hoffmann and Sgro2011, Pandolfi et al. 2011), such studies are rare inmarine systems, and nonexistent for macroalgae.Clark et al. used genetic breeding design experi-ments to assess whether there was genetic variation

in thermal sensitivity between two populations of ahabitat-forming intertidal fucoid, Hormosira banksii.They demonstrated how thermal reaction patterns(plots of performance vs. temperature for eachgenotype; Fig. 1) can be used to illustrate geno-type–environment interactions in developing algalembryos (as proposed for terrestrial insects by King-solver et al. 2004) and thereby identify the potentialsusceptibility of populations to climate change. Theinfluence of genotype on environmental toleranceand the potential for adaptation to environmentalstress has not previously been examined for marinealgae, but, as this study showed, may be important.Fucoid algae are conspicuous habitat-formers on

temperate intertidal reefs globally (Fig. 2a), and atleast some of these species have been demonstratedto act as autogenic engineers (Jenkins et al. 1999,Jenkins et al. 2004, Schiel 2006, Lilley and Schiel2006). There is evidence from south-eastern Austra-lia that extreme temperature events can cause sun-burn (Fig. 2b) and significant canopy loss of theintertidal fucoid, Hormosira banksii, and associatedchanges to mid-shore communities (Keough andQuinn 1998). Changes to the distribution and abun-dance of autogenic engineers, such as H. banksii inthe intertidal (and various laminarian and fucoidspecies in the shallow subtidal), can have cascadingand long-lasting effects on the structure, diversity,and resilience of associated communities (Jenkinset al. 2004, Schiel 2006, 2011, Johnson et al. 2011,Schiel and Lilley 2011, Wernberg et al. 2011a).Understanding the connectivity, genetic diversity,and differences in temperature tolerance (Wern-berg et al. 2011b) of important intertidal and sub-tidal habitat-forming species, in the context of theirbroader geographical distributions, will be impor-tant for assessing the capacity of these species (andtheir associated communities) to adapt to future airand sea temperature profiles.Projected sea-surface temperature changes will

not happen in isolation. It is the cumulative effectsfrom a range of interacting processes that will havethe greatest impacts on existing ecosystems, but willalso be hardest to predict (Russell et al. 2009,Russell et al. 2012). For example, the effects of

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temperature on the physiology of organisms willaffect their responses to extreme events such asstorms, which might include storm surges, floodingand increased turbidity, large run-off events withassociated water quality changes as well as physicaldisturbance caused by increased wave action. Fur-thermore, the ability to recover or recolonize anarea following the combined effects of climate-related events might depend on the delivery ofpropagules by the prevailing currents, nutrient avail-ability that might be impacted by changes to upwell-ing regimes, and the effects of ocean acidificationon early life stages of available organisms (Fabryet al. 2008). Climate-driven changes also need to beconsidered in the context of other anthropogenic

stressors and influences, such as overfishing (Linget al. 2009a), invasive species, pollution (Bellgroveet al. 1997, Brown et al. 2000), urbanization, andengineered coastlines (Airoldi et al. 2005). Thepotential synergies amongst such multiple stressorsare only just beginning to be examined. Clark et al.(2013) demonstrated that consideration must begiven to the within- and between-population geneticvariations specifically to individual and multiplestressors, in addition to understanding the averageeffects of given stressors in isolation and combina-tion. Macroalgae with easily manipulated gametes(such as fucoids) provide good model systems totest these ideas, as may cultures of microalgal spe-cies with short generation times. Moreover, theimportance of habitat-forming macroalgae for mar-ine biodiversity and the role of marine algae in theglobal carbon cycle highlight the need for a greaterunderstanding of the factors influencing their sensi-tivity and adaptability to environmental and anthro-pogenic stress.

ALECIA BELLGROVE

Centre for Integrative Ecology, School of Life &Environmental Sciences, Deakin University,

Warrnambool, Victoria 3280, AustraliaE-mail: alecia.bellgrove@deakin.edu.au

Airoldi, L., Abbiati, M., Beck, M. W., Hawkins, S. J., Jonsson, P.R., Martin, D., Moschella, P. S., Sundelof, A., Thompson, R.C. & Aberg, P. 2005. An ecological perspective on thedeployment and design of low-crested and other hard coastaldefence structures. Coast. Eng. 52:1073–87.

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FIG. 1. Thermal reaction norms of performance of differentgenotypes (represented by each line) exposed to control and ele-vated temperatures. Nonparallel and/or overlapping lines indi-cate genotype–environment interactions illustrating geneticvariation in performance with temperature, whereas parallel linesindicate temperature-independent variability in performance.Based on Clark et al. (2013) and Kingsolver et al. (2004).

(a) (b)

FIG. 2. (a) The fucoid alga, Hormosira banksii, forms extensivecanopies dominating the rocky intertidal of temperate Australasiafrom Albany, Western Australia to northern New South Wales,around Tasmania, the North and South Islands of New Zealandand some of the smaller offshore islands in southern Australasia;(b) during intense and prolonged periods of high temperatureand UV exposure the thallus of H. banksii can become sunburnt.Oxidized phenolic compounds are released from physodes in theperipheral cells and protect the photosynthetic tissue beneath(Schoenwaelder 2002), but, in extreme cases, can lead to tissuedeath and significant canopy loss (Keough and Quinn 1998).Photographs courtesy of Jennifer Clark, University of Technology,Sydney.

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