Algal%20Ecology.pdf

Algal Ecology Robert E DeWreede, University of British Columbia, Vancouver, Canada Algal ecology is the study of the distribution and abundance of algae, of the environment in which they exist, and of the interactions between the algae and with other organisms. Introduction The eukaryotic algae are, in general, aquatic, photosyn- thetic organisms with a simple morphology (lacking the complextissuesofvascularplants),andwithreproductive structures inwhich all cells formspores or gametes. Both unicellularandmulticellularspeciesexist,andtheymayor maynotbe?agellated.Thedistributionandabundanceof algae is determined by physical factors such as light, temperature,salinityandwatermotion,andbybiological factorssuchasherbivoryandcompetition,andbycomplex interactionsbetweenthesevariables. Habitats and Adaptations (Eukaryotic Algae) Algae have been found in almost all environments where humans have been able to explore. In extreme environ- mentssuchashotthermalspringsanddeserts,prokaryotic ?algae? (nowclassi?ed with thebacteria) arepresent.Less extreme environments, e.g. snow ?elds, underneath polar ice, cooler hot spring waters and aerial environments, supportsomeeukaryoticalgae. Algae cope with environmental stress in many ways. Some green algae such as Chlamydomonas nivalis (Chlor- ophyta,snowalgae)produceprotectivepigmentstoshield the chloroplasts from intense sunlight. The giant kelp Macrocystis(abrownalga;Heterokontophyta),whichcan attain lengths of over 30m, has specialized tissues for moving energy-rich compounds from the light-saturated blades to the basal parts that may lack su?cient light for photosynthesis. Eveninlessextremehabitatsalgaecopewithavarietyof physicalstresses.Inlatesummerintemporarypondsand smalllakesdesiccationmayoccur.Here,somemembersof the Volvocales (Chlorophyta) produce resistant stages, which can survive drying until water once more accumu- lates.Inmarinewaters,highintertidalspeciesofPorphyra (Rhodophyta;redalgae),oftendryoutsomuchthatthey crumble to the touch; yet, once rewetted by the incoming tide,theyresumenormalmetabolicprocesseswithin20]30 minutes. Biological factors are also important determinants of algal abundance. Some tropical algae such as species of Halimeda(Chlorophyta)producetoxiccompoundswhich reducegrazingby?sh(PaulandvanAlstyne,1988).Many of the larger brown algae produce phloroglucinol-like compoundswhichdetergrazingbyseaurchinsandchitons (Paul, 1992). Some algae are thought to have evolved complexlifehistoriesinordertoavoidexcessiveherbivory. For example, red algae such as Mastocarpus alternate between a bladed phase which produces gametes and a crustose phase producing spores. The crustose phase is moreresistanttosomeherbivoressuchaschitons,butthe bladesarebettersuitedforthedisseminationofreproduc- tivestructures. Marine versus Freshwater Algae exist in freshwater and marine habitats, both in constantly submerged sites and in areas periodically covered by water. In freshwater habitats such periodic emersion may occur as a result of seasonal drought; in marinewatersitisduetotidalcycles.Freshwaterhabitats are usually the domain of smaller algae, such as micro- scopic green algae, euglenophytes, diatoms, chrysophytes and dino?agellates; brown and red algae are rare. In contrast, in marine habitats, larger algae (seaweeds) such asbrownandredalgaeareverycommon,asarethelarger green algae; euglenoids, diatoms, dino?agellates and haptophytescanalsobefoundthere. Ingreenalgaeinhabitingfreshwater,environmentalcues suchasfallingwaterlevelsinadryingpondmayinitiatethe productionofsolubleorganicchemicalscalledpheromones bysomeindividuals.Thesepheromonestriggertheforma- tionofreproductivestructuresandeventuallygametes,and alsoattract?agellatedspermcellstothenonmotileegg.The productofsexualreproductionisoftenaresistantstage,a stageusuallylackinginmarinegreenalgae. Euglenophytes (Euglenophyta) may occur in ponds on agricultural lands, and as sand-dwelling species on some marine beaches. Euglenophytes have ?eyespots? which, in Article Contents Secondary article . Introduction . Habitats and Adaptations (Eukaryotic Algae) . Marine versus Freshwater . Subaerial Algae . Extreme Environments . Thermal Springs . Snow and Ice . Zonation . Blooms . Fish-eating Dinoflagellates (Pfiesteria) 1ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net conjunctionwithalight-sensitivesiteatthebaseofoneof the ?agella, enable them to move in response to light direction. Diatoms (Heterokontophyta) are single-celled algae withawallofsilica.Therearetwodistinctdiatomgroups: pennate diatoms are generally symmetric about a central lineandusuallyattachedtoasubstratum;centricdiatoms are symmetrical about a central point and usually free ?oating. Diatoms mostly lack ?agella but movement can occur in those pennate diatoms that are attached to a substratum and possess a raphe. Centric diatoms are planktonic and are a major contributor to open ocean productivity. Chrysophytes (Heterokontophyta) and dino?agellates (Dinophyta)occurinbothfreshwaterandmarinehabitats. Chrysophytes are ?agellated unicells, often a golden- brown colour due to pigments such as xanthophylls and carotenoids.Somearethepredominantspeciesinnutrient- poor alpine lakes. Dino?agellates areresponsible (in part or entirely) for a multitude of phenomena, including bioluminescence, red tides, shell?sh poisoning and cigua- tera. Dino?agellates also occur in corals, where they contribute signi?cantly to their growth. The colour of dino?agellatesvariesfromgreenishhuestoshadesofred, andmanyspecieslackchloroplasts.Intheselatter,feeding often occurs by ingesting small cells, or by liquefying the ?eshofprey(seeP?esteria,below). Bioluminescence occurs in some dino?agellates (e.g. NoctilucaandPyrocystis)bymeansofthesamechemicals (luciferan and luciferase) used by some other organisms withbioluminescentorgans,suchas?sh(Sweeney,1987). Bioluminescence may be a means of startling herbivores. Many dino?agellates produce toxins, although the pur- poseofthisisunclearsincetheimmediateconsumerofthe toxiccell,e.g.a?lterfeedersuchasaclamormussel,isnot a?ected. Asmentionedabove,redalgae(Rhodophyta)arerarein freshwater habitats, and common in marine ones. They haveno?agellaatanystageoftheirlifehistory,andthus do not make use of pheromones in sexual reproduction. The life history of many red algae, with alternating gametophyte (haploid) and sporophyte (diploid) stages, is made more complex in many of its species by an additional life history stage, the carposporophyte which forms diploid spores. This is one way in which red algae apparentlymaximizetheproductionofo?springwhenever sexual fusion occurs. Many red algae also produce phycolloids (e.g. carrageenans and agars) as part of their cell walls. These chemicals are complex, sulfated, long- chaincarbohydratesusedwidelyinthefood,chemical,and pharmaceuticalindustry.Thefunctionofphycocolloidsin these algae is not known, but they may facilitate the retention of water during low tide, and discourage the settlementofepiphytes. Brownalgaearealsorareinfreshwater,butoftenarethe most visible algae in temperate and tropical seas. Brown algaelackanyunicellularindividuals,exceptforthespores and gametes. Pheromones play an important role in promotingsuccessfulsexualreproductionforsomebrown algae.Chemicalanalysesofbrownalgalpheromoneshave shownthateachalgalspecies(e.g.kelpssuchasspeciesof Laminaria and Alaria) secretes several pheromones (a ?bouquet?; Maier and Mušller, 1986) which are not always species speci?c. Hence a sperm cell of one species maybeattractedbythepheromonessecretedbytheeggof another species. In this case, species speci?city is ensured by proteins that coat the egg, and which must be ?recognized?bythespermcell. The haptophytes (Haptophyta) are a group of unicel- lular algae with two ?agella and a haptonema (an extensible structure between the two ?agella) which may facilitate feeding or attach the organism to a substrate. Somehaptophytesformimmenseopenoceanblooms. Subaerial Algae Subaerial algae may be found on leaves, tree trunks, muddy banks, on or beneath the surface of soil, and on brickwalls.Onwallsandtreetrunksthesealgaeformdusty greenstreaksofcolourdi?culttodistinguishfromlichens and bryophytes. Species of the green algal family Chlorococcaceae, and speci?cally the genus Chlorococ- cum,arecommoninthesehabitats.SpeciesofChlorococ- cum are simple, round cells capable of reproducing both asexually (by zoospores) and sexually. Some species are remarkably resistant to desiccation, possibly due to their thickcellwallswhichformunderdryconditions.Agreen soil alga, Zygogonium ericetorum, produces a purple pigment which colours the soils of heaths in parts of the UK. Extreme Environments Despite their fragility, algae also occur in extreme environments.Onegreenalgaethatthrivesinhighlysaline habitats,e.g.saltponds(normalsalinityinseawaterranges from 2.8 to 36%; salt ponds may even form a brine (asaturatedsaltsolution)),isDunaliellasalina.Thisspecies produces both b-carotene (a yellow-orange pigment), to shield the alga from excess light, and glycerol, which counteracts the osmotic potential of the highly saline water. Industrial production of this alga occurs, for example in Australia, where both the pigment and the glycerol are extracted from cultured Dunaliella (Borowitzkaetal.,1986). Anotherextremeenvironmentisfoundinminetailings, ortheareasa?ectedbythedrainagefromsomeminesites, which may contain high concentrations of copper, cadmium, iron, etc. In addition, acids may form if the Algal Ecology 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net tailingscontainsulfatedminerals;theseacidsinturnleach moreheavymetalsfromtherock.Freshwaterorganismsin such environments su?er from both the low pH and the metals.LowpHdoesnota?ectmarinewatersasmuch,due to their bu?ering capacity, and heavy metals may ?occulatebycomplexingwithorganicparticles.Onestudy of acid mine drainage (AMD), at Britannia Mines in British Columbia, Canada, reported that an area up to some500moneithersideofacreekcarryingtheAMDwas devoid of algae. Further away, some unicellular green algae appeared, then a multicellular green seaweed Enteromorpha, followed by the brown seaweed Fucus. TransplantstudiesofFucusfromnona?ectedsitestosites impacted by AMD showed an increase in copper concentration from 5 500ppm Cu (dry weight) at day 0 to 2400ppm at day 40 (Marsden, 1999). The ability of Enteromorpha to tolerate some heavy metals was also notedinstudiesonAMDinChile. Some algae tolerate metals by avoiding them, e.g. the diatomAchnanthessp.,whichgrowsonagelatinousstalk andhenceawayfromsuchhighcoppercontentmaterialsas antifouling paints on ships. Other diatoms, Navicula and Amphora, apparently detoxify copper internally by com- plexing it with organic compounds. The brown alga Ectocarpus siliculosus has both copper tolerant and resistantstrains;theresistantstrainsexcludemorecopper thannonresistantstrains. Thermal Springs Thelocationandabundanceofalgaeinthermalspringsare determined predominantly by temperature and dissolved mineralgradients.Higherwatertemperatures(over608C) favour cyanobacteria, whereas eukaryotic algae such as Cyanidium caldarium have upper temperature limits around 55]578C (Darley, 1982). Tolerance to such high temperatures is due in part to the high melting point of algalmembranelipids,andtheincreasedthermalstability of algal proteins. Diatoms also occur in hot springs, especially at temperatures between 30 and 408C; Ach- nanthesexiguahasatemperaturemaximumof448C,anda minimum at 108C. At lower temperatures (20]308C) the green alga Zygogonium mayform purplebands of colour (duetoaniron]tannincomplexstoredinvacuoles)insome springs. This species also prefers acid waters, tolerating a pHfrom1to5. Snow and Ice Somealgaemaketheirhomeonsnowandice.Patchesof red, orange, yellow and green colours on alpine snow are oftencausedbyalgaesuchasChlamydomonasnivalis,and speciesofChloromonasandChlainomonas,allgreenalgae (Hoham,1980)growinginthemeltwaterontopofsnowor ice.Similartotheirsalt-tolerantrelativeDunaliella,many of these algae produce carotenoid pigments, e.g. astax- anthin, reducing photodegradation of the chlorophyll pigments. Snow algae are present as dormant zygotes for most of the year and only reproduce sexually in the meltwater. C. nivalis has a growth optimum at 5108C, andcanphotosynthesizeat08C. Zonation Zonation refers to the existence of zones of organisms in marine intertidal and subtidal environments. Zonation is sometimes obvious in intertidal habitats, but often much lesssosubtidally.Varioustheorieshavebeenproposedto accountforzonation,rangingfromphysicalcausessuchas ?tidefactors?,tobiologicalonessuchasherbivory. The tide factor hypothesis, and its variants, proposes thatzonationresultsfromdi?erentialtolerancesofmarine organisms to desiccation and temperature, generated by theriseandfallofthetides.Tidalpatternsdi?eraroundthe world, and can be diurnal, semidiurnal or mixed semi- diurnal. Since the extent of the intertidal area covered by anytidecanvaryfromdaytoday,especiallywheremixed semidiurnal tides occur (as in the Eastern Paci?c), any given elevation may be exposed to air from minutes to hours on di?erent days, and from hours to weeks over a month.Thus,elevationsonlyafewcentimetreshigherthan another site could be subjected to additional hours of exposure to air over a 24-hour period. However, the correlationbetweensuch?breaks?intimesofairexposure andactualzonalboundariesispoor. Factors such as competition and herbivory have also been proposed to account for zonation. Since biological diversity increases in the lower intertidal zone (compared tothehigherintertidal)biologicalfactorsmayincreasein importance in lower elevation sites. Experiments manip- ulatingthenumbersofherbivoresorpredatorshaveshown thatsomeofthesehaveasigni?cantimpactontheextentof a particular zone. For example, removal of Pisaster,a predatory star?sh, results in extending the lower limit of the zone of mussels (Mytilus calfornianus); the mussels in turnovergrowthealgae,thusloweringtheupperextentof thealgalzone. The physiological properties of algae clearly play a centralroleintheirtolerancetodesiccation.Theabilityof somePorphyraspeciestotolerateextremedesiccationhas already been mentioned. A green alga, Prasiola meridio- nalis, which exists higher in the intertidal zone than Porphyra, can tolerate days of desiccation and high temperatures. Some species, e.g. Fucus gardneri, a brown seaweed found high in the intertidal zone, can photo- synthesizeinair(Quadiretal.,1979),althougheventually nutrient stores are depleted, as these cannot be obtained Algal Ecology 3ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net fromair.Forsomedesiccatedalgae(e.g.Fucus,Ulvaand Gracilaria), it has been found that nutrient uptake rates upon reimmersion in seawater are positively related to increasing elevation in the intertidal zone (Thomas et al., 1987).Thus,somehigherelevationalgaenotonlycanhave apositivenetphotosynthesisinairbutalsoarecapableof replenishingnutrientpoolsquickly. Subtidalzonationhasalsobeendescribed.Thecauseof zonation here has been attributed to at least two possible factors: the change in the composition of available light and the change in light intensity with increased depth. Becauseofthematerialsdissolvedinseawater,redlightis generally absorbed within the ?rst few metres from the surface; blue light penetrates deepest. Since the di?erent groups of algae have di?erent pigments and thus utilize di?erent portions of the visible spectrum optimally, one theory explainedthe allegeddeep occurrence of redalgae bytheirabilitytomakeuseofbluelight,andtheapparent absenceofgreenalgaeatsuchdepthsbytheirinabilityto utilize this part of the spectrum as e?ciently. The second theoryattributedthepresenceofalgaeatdeeperdepthsto their ability to simply absorb light, i.e. some algae were arguedtofunctionbetterorworseasa?blackbody?.More recent experiments have supported the latter theory (Ramus, 1983). That light absorption capacity controls depth of occurrence was given further credence by more detailedstudiesofdeep watercollections; thereis amuch less clear pattern of zonation by pigment group than had beenalleged,anddeepalgaecanbegreen,redorbrown. Intertidal zone The abundance and distribution of intertidal algae are determinedbyamixofphysicalandbiologicalfactors,and bythephysiologicalpropertiesoftheindividualspeciesof algae. Some of the physical factors that are important in this respect have been mentioned above, e.g. desiccation, temperature and salinity. Higher temperatures(27]308C) canresultinhigherratesofrespirationandabreakdownof photosyntheticmechanisms.Speci?csdependofcourseon the individual species. Both increased and decreased salinity (relative to the normal range the species encoun- ters, usually 25]36%) also results in increased rates of respiration.Thus,thecombinationofhighertemperatures and lower salinity can be particularly stressful to marine algae.Anotherphysicalfactoristhee?ectofwaveimpact onseaweeddistribution.Therelationshipbetweenthedrag andaccelerationforcesgeneratedbymovingwater,anda seaweed?smorphology,physicalstrengthandtheforceof attachment,hasbeenshowntoa?ectthallusshape,surface areaandabundance.Someseaweedscopewiththeimpact of increased water movement by reducing surface area, and increasing elasticity; for example, a species with wide blades, Mazaella splendens (a red seaweed), was replacedbyacloselyrelatedspecieswithnarrowerblades, M. linearis, in sites of relatively higher wave impact (Shaughnessyetal.,1996). Subtidal zone Some of the same biological factors that in?uence the abundanceanddistributionofintertidalseaweedsalsoact in the subtidal zone, e.g. competition and herbivory. Competition may occur for substrate and light; common herbivores in the subtidal zone are sea urchins and, in tropical seas, also herbivorous ?sh. Sea urchin food preferencestudieshaveshownanavoidanceofsomealgae, andapreferenceforothers.Avoidanceisusuallyattributed to comparative toughness and to unpalatable chemicals. Forexample,temperatewatergeneraofbrownalgaesuch as Agarum and Laminaria, and tropical green seaweeds such as Halimeda, produce compounds (usually phlor- otannins in brown algae and other complex organic compounds in Halimeda) which are strong deterrents to herbivores (Paul and van Alstyne, 1988). Some of these algae are recognized by ?sh as unpalatable; this bene?ts adjacentpalatablespeciesofalgaewhicharealsoavoided by grazing ?sh; an example of a positive interaction. ExtensivestudiesofHalimedahaveshownthatthisspecies hasamixofstoredantiherbivorecompounds,andthatthe actofherbivorycanresultintheconversionofalesstoxic compound into a more toxic one. It is not clear whether herbivory itself induces the formation of antiherbivore compounds. Studies on Fucus indicate that such com- pounds do form in response to herbivory (van Alstyne, 1988),butsimilarstudiesusingotheralgaehavenotfound thistobethecase(Steinberg,1994). Asalreadyindicated,di?erentphysicalfactorsdi?erin ecologicalimportanceintheintertidalandsubtidalzones. Desiccation is absent in the subtidal, and the marked variationsinsalinityandtemperaturethatcanoccurinthe intertidal zone are much less likely to occur subtidally. Light plays a role in limiting the depth at which di?erent speciesofalgaeoccurinthesubtidal,andexcesslightlimits some intertidal seaweeds. In the shallow subtidal, wave actionisimportant,asitisintheintertidalzone. Blooms Algal blooms are concentrations of (usually) unicellular algae,wellabovetheirnormalconcentrations(e.g.210000 cellsL 21 in a bloom of the dino?agellate Gymnodinium mikimotoi). Blooms may consist of primarily a single species of algae, or of several; some blooms consist of di?erent species over time as species succession occurs. Bloom-forming species are diverse, e.g. Gyrodinium spp., Alexandrium spp., Gonyaulax spp., Gymnodinium spp. (dino?agellates), Heterosigma akashiwo (Raphido- phyta), Emiliana huxleyi and Prymnesium (parvum?) Algal Ecology 4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net (Haptophyta), Pseudonitzschia australis (Bacillariophy- ceae),andAureococcusanaphage?erens(Chrysophyceae). Conditions that favour the formation of blooms are relatively calm, clear waters, and increasing light and nutrient levels. Such conditions are more likely inspring- time, following the activities of winter and early spring storms. Bloomsareoftendescribedonthebasisofcolour.White blooms caused by Emiliana huxleyi have occurred over immenseareasoftheNorthAtlanticsouthofIcelandand elsewhere(vandenHoeketal.,1995).Thewhitecolouris causedbythealga?scalciumcarbonatescales,whichhave also been identi?ed as an important sink for carbon dioxide.Somedino?agellates,e.g.Gymnodiniumsp.,create olive-green blooms, and produce a toxin that causes stinging in the eyes and respiratory discomfort. Other dino?agellates,e.g.Gonyaulaxcatenella andG.tamarensis, are responsible in part for ?red tides?, and various species cause paralytic or diarrhoetic shell?sh poisoning. Cigua- tera(theaccumulationoftoxinsby?sh)isalsoattributed to dino?agellates, in this case a species associated with tropical algae eaten by herbivorous ?sh. Brown tides are often the result of diatom blooms; domoic acid, a toxic chemicalproducedbyPseudonitzschiaaustralis,hasbeena threat in the northeastern USA, where it was responsible for brain damage and human deaths. Apart from direct e?ectsonhumans,algalbloomsalsocauseimmenseharm to shell?sh and ?n-?sh aquaculture operations. Some diatom species (e.g. Chaetoceros sp.) damage the gills of ?sh with their silicon spines. In 1998, blooms of the dino?agellate Gymnodinium mikimotoi resulted in the deathofatleast1500tonnesof?shinHongKong,about halftheamountof?shproducedtherein1997.Estimates of ?nancial losses ranged from US$10.3 million (govern- ment estimate) to US$30 million (farmer?s estimate) (LuandHodgkiss,1999). Harmfulbloomsareseenmorefrequentlytoday,andin placeswheretheyhavebeenrarelyseeninthepast.Factors held responsible for this are increased awareness, eutro- phication from agriculture, transfer of toxic organisms around the globe by ship?s ballast water, and possibly increased run-o? due to deforestation. Deserti?cation in the Sahara may be contributing to blooms of Emiliana huxleyi in the Mediterranean, as desert dust provides mineralsrequiredbythisalgae. Fish-eating Dinoflagellates (Pfiesteria) The ?cell from Hell? is the term that has been used to describethedino?agellateP?esteriapiscicida.In1991itis estimatedthatatleastabillion(1 C2 10 9 )?shwereloston theeastcoastoftheUSA,andin1995perhaps10million, due to P?esteria. The toxin it produces is lethal to ?sh (causingseverelesionsanddeath)andtohumans(causing nausea and memory loss so severe it mimics Alzheimer disease). P?esteriahasanunusuallycomplexlifehistoryofsome 24 di?erent stages varying from a cyst which lies on the mud, to amoeboid stages, predatory forms which release toxinsthatcanresultinulceratingsoreson?sh,andother forms capable of consuming the ?esh of the dead ?sh (BurkholderandGlasgow,1997).Anaddedfeatureisthat one of the stages, a nontoxic zoospore, grazes on other algae and is able to retain the prey chloroplasts for some time as functional organelles. Thus, this normally non- photosynthetic organism can have at least one photosyn- thetic stage, apparently making it less dependent on prey (Lewitusetal.,1999).Actionshavebeeninitiatedtoreduce e?uents which, it is hoped, will reduce the incidence of suchbloomsinareassuchasChesapeakeBay,USA. References BorowitzkaLJ,MoultonTPandBorowitzkaMA(1986)Salinityandthe commercial production of beta-carotene from Dunaliella salina. In: Barclay WR and McIntosh RP (eds) Algal Biomass Technologies, an InterdisciplinaryPerspective.NovaHedwigia 83:224]229. Burkholder JM and Glasgow HB Jr (1997) The ichthyotoxic dino- ?agellate,P?esteriapiscicida:behaviour,impacts,andenvironmental controls.LimnologyandOceanography 42:1052]1075. Darley WM (1982) Algal Biology: A Physiological Approach. In: WilkinsonJF(ed)BasicMicrobiology.Oxford:BlackwellScience. HohamRW(1980)Unicellularchlorophytes ] snowalgae.In:CoxER (ed)Phyto?agellates,pp.61]84.Amsterdam:Elsevier. LewitusAJ,GlasgowHBJrandBurkholderJM(1999)Kleptoplastidy in the toxic dino?agellate P?esteria piscicida (Dinophyceae). Journal ofPhycology 35:303]312. Lu Songhui and Hodgkiss IJ (1999) A Gymnodinium mikimotoi occurrencespring1998.HarmfulAlgaeNews 18:2-3. Maier I and Mušller DG (1986) Sexual pheromones in algae. Biological Bulletin(WoodsHole) 170:145]175. Marsden AD (1999) The e?ects of acid mine drainage at Britannia Beach, B.C. on Fucus gardneri and associated intertidal algae. MSc thesis, Department of Botany, The University of British Columbia, Vancouver,Canada. PaulVJ(1992)EcologicalRolesofMarineNaturalProducts.Ithaca,NY: ComstockPublishing. PaulVJandvanAlstyneK(1988)AntiherbivoredefensesinHalimeda. Proceedings of the 6th International Coral Reef Symposium, pp. 133]138.Australia. Quadir A, Harrison PJ and DeWreede RE (1979) The e?ects of emergenceandsubmergenceonthephotosynthesisandrespirationof marinemacrophytes.Phycologia 18:83]88. Ramus J (1983) A physiological test of the theory of complementary chromaticadaptation.II.Brown,green,andredseaweeds.Journalof Phycology 19:173]178. Shaughnessy FJ, DeWreede RE and Bell EC (1996) Consequences of morphology and tissue strength to blade survivorship of two closely related Rhodophyta species. Marine Ecology Progress Series 136: 257]266. Steinberg PD (1994) Lack of short-term induction of phlorotannins in theAustralianbrownalgaeSargassumvestitumandEckloniaradiata. MarineEcologyProgressSeries 121:129]133. Algal Ecology 5ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net SweeneyBM(1987)Bioluminescenceandcircadianrhythms.In:Taylor FJR (ed) The Biology of Dino?agellates, pp. 269]281. Oxford: Blackwell. ThomasTE,TurpinDHandHarrisonPJ(1987)Desiccationenhanced nitrogen uptake rates in intertidal seaweeds. Marine Biology 94: 293]298. van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown algae Fucus distichus. Ecology 96: 655]663. van den Hoek C, Mann DG and Jahns HM (1995) Algae: An IntroductiontoPhycology.Cambridge:CambridgeUniversityPress. Further Reading Anderson DM (1995) Toxic red tides and harmful algal blooms: a practicalchallengeincoastaloceanography.ReviewofGeophysics 33 (suppl.):1189]1200. KingsfordMandBattershillC(eds)(1998)StudyingTemperateMarine Environments: A Handbook for Ecologists. Christchurch, New Zealand:CanterburyUniversityPress. Van den Hoek C, Mann DG and Jahns HM (1995) Algae: An Introduction to Phycology. Cambridge: Cambridge University Press. Algal Ecology 6 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net A0317 1..6