Protozoan%20Ecology.pdf

Protozoan Ecology O Roger Anderson, Columbia University, Palisades, New York, USA Protozoan ecology is the interaction in space and time of protozoa (flagellates, amoeboid organisms and ciliates) with other living organisms and the physical environment. It encompasses, among other factors, sources of food and energy used to sustain life, food web dynamics, the role of protozoa in maintaining fertility of ecosystems, and adaptive strategies for survival in varying habitats. Introduction Thefree-livingprotozoadwellingintheopenenvironment (as opposed to parasitic forms invading other living organisms) include ?agellates, amoeboid organisms and ciliates (Figure 1). Only free-living protozoa will be consideredhere. Flagellatesmovebyawhip-likemotionofoneormore ?agella (slender, undulating membrane-enclosed projec- tions)protrudingfromthecellbody.Itiswidelyaccepted that protozoa originated from a primitive ?agellate stock andthatallothergroupsoffree-livingprotozoa,including sarcodines (amoeboid organisms) and ciliates, evolved from primitive ?agellated organisms. Amoeboid organ- ismsmovebycytoplasmic?ow,typicallyusingspecialized pseudopodia (?nger-shaped, elongated pencil-shaped or net-like cytoplasmic protrusions). Some species form ?agellated stages during reproduction or dispersal. The sarcodines include naked and shell-bearing (testate) amoebae, heliozoa (the so-called sun animals with a coronaofradiatingaxopodia),andmarineformsincluding foraminifera (with calcite shells), radiolaria (some with siliceousornateshells)andacantharia(secretingstrontium sulfate skeletons). The naked amoebae or gymnamoebae includethecommonlyrecognizedAmoebaproteus.Altho- ugh this species is often used in teaching demonstrations, it is much larger (c. 500mm) than most naked amoebae, whichareusually20mmorlessinlength.Nakedamoebae lacksubstantial surface covering. However, some species have an organic surface coat (glycocalyx) or layer of organic scales secreted on the surface of the membrane. Testate amoebae are enclosed within an organic or mineralized shell with a terminal aperture. Pseudopodia usedforlocomotionandfoodgatheringprotrudefromthe aperture. Ciliates move by the coordinated motion of numeroushair-likeciliawhosebeatingmotionpropelsthe ciliate through the water. Some use specialized groups of sti?enedventralcilia,calledcirri,for?walking?onsurfaces. Ciliates are believed to be the most evolutionarily advanced group of protozoa. They possess two kinds of nuclei, a large macronucleus and one or more smaller micronuclei,amajortaxonomicfeature.Theyaretypically particlefeeders,althoughsomepreyon?lamentousalgae andotherslackanorganizedfeedingapparatus.Thelatter obtainnutritionbyabsorbingsolublefood. Photosynthetic (autotrophic) species occur among the ?agellates,butmany speciesof ?agellatesandmostother protozoa are nonphotosynthetic (heterotrophic) and obtain food from the surrounding environment, either as soluble organic molecules or as particulate food ingested by the cell. Some ciliates gather chloroplasts that are segregatedfromingestedalgaeandusethemasasourceof intracellular photosynthesis. These chloroplasts are not permanent and are eventually lost, necessitating further replenishment from ingested algae. Species with both photosynthetic and heterotrophic modes of nutrition are termed mixotrophic. An interesting example is the ciliate Myrionecta(formerlyMesodinium)rubrumwhichcontains algal symbionts. Some sarcodines, including gymnamoe- bae,foraminiferaandradiolaria,formalgalsymbiosesand obtainpartoftheirnutritionfromphotosynthatesreleased bythealgae.Manyofthesesymbiont-bearingspeciesalso requireadditionalsourcesofparticulatefood(microorga- nismicandinvertebrateprey)gatheredfromthesurround- ingenvironment. Highly diverse feeding strategies have evolved among heterotrophic protozoa to capture particulate food, including mechanisms for snaring and ingesting a wide variety of microorganisms and small invertebrates Article Contents Secondary article . Introduction . General Survey . Roles in Ecosystems . Specialized Habitats . Life Cycles Figure 1 Protozoa: (a) flagellate, Polytoma uvella (15 mm); (b) gymnamoeba, Metachaos discoides (400 mm); and (c) ciliate, Phacodinium metchnikoffi (100mm). Reproduced with permission from Lee JJ, Hutner SH and Bovee EC (eds) (1985) Illustrated Guide to the Protozoa. Lawrence, KS: Society of Protozoologists. 1ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net (seeGeneralSurvey).Speciesoffree-livingprotozoavary insizefromafewmicrometrestohundredsofmicrometres, and the larger sarcodines (foraminifera and solitary radiolaria) reach dimensions of several millimetres. Fila- mentous colonial forms of radiolaria (containing up to hundreds of cells or more), with individual diameters of onlyseveralmillimetres,reachlengthsofametreormore! Increasingevidencepointstoacriticalroleofprotozoain stimulating productivity of communities of microorgan- ismsandtheenhancementofthestabilityandproductivity offoodwebsthroughmineralizationofessentialnutrients thatpromotegrowthofhigherorganismsatupperlevelsof food webs. Some of these signi?cant contributions of protozoainthedynamicsofecosystemsarepresented. General Survey Protozoa occur in widely diverse aquatic and terrestrial habitatsworldwide,spanningthedarkdepthsoftheocean to the sun-splashed, snow-covered peaks of the highest mountains. With improved methods of detecting and enumeratingsomeofthemoredelicateprotozoanspecies (especially the small gymnamoebae), we are gathering increasingevidenceoftheirnumericalimportanceinmany habitatswheretheyhavepreviouslybeenoverlooked(e.g. Anderson and Rogerson, 1995; Darbyshire etal., 1996). Gymnamoebae in highly productive ponds reach max- imum abundances of over one million per litre, and in marine coastal water occur in thousands per litre. Ciliate maximum abundances reach hundreds of thousands per litre in subtropical lakes. In soils, the total number of protozoapergramatahighlyproductivesitewasfoundto be 162400, of which 123000 were amoebae, 27300 were ?agellates and 12100 were small ciliates (Foissner, 1987; Darbyshire, 1994, p.52). Abundance and diversity of protozoa are determined by physical environmental (abiotic)andbiological(biotic)factors.Weexaminesome abioticandbioticfactorsinprotozoanecology. Abiotic factors Importance of water Living cells contain as much as 80% water, which is essential for metabolic life-sustaining processes. Many speciesofprotozoalacksubstantialsurfaceprotectionand depend on an abundant supply of moisture during active stagesoffeedingandgrowth.However,manyarecapable of forming cysts during drought or other unfavourable conditions. Many freshwater species of protozoa also occurinterrestrialenvironmentsandhavebecomeadapted toformrestingstagesorcystsduringintermittentperiods of water depletion. Terrestrial environments are particu- larlysusceptibletounfavourablegrowthconditionsdueto lackofmoisture,eitherthroughperiodicdryingordueto binding of the water in thin ?lms on surfaces or within microspacesinthesoil.Thiswaterisboundsostronglythat protozoacannotcompeteforitosmotically.Ingeneral,it hasbeenestimatedthatawater?lmthicknessof3mmisthe ultimate lower limit for protozoan activity (Albouvette etal.,1981),andbelowthisrangetheprotozoadieormust encyst to survive. The smaller the species, the thinner the ?lm of water required for subsistence. The small ciliate Colpodasteinii (c.20mm) is active only if the water ?lm thickness is approximately 30mm (Darbyshire, 1976), while small amoebae can undoubtedly tolerate thinner water?lms(Fenchel,1987).Theamountofwaterboundis expressed in pressure units, e.g. bars (1bar=10 6 dy- nescm 22 ), equivalent to the amount of suction required toremovewaterfromasoilsample.Therelationbetween pressure (h in bars) and pore size (d in mm) is: h=3/d. Temperate soils when fully moistened (?eld capacity) containapproximately30?50%water(althoughthismay vary at di?erent geographic locations) and have a water suctionofabout50mbar.Thiscorrespondstoaporesize of about 60mm, an amount su?cient to sustain active protozoa.Bycontrast,tropicalsoilsat?eldcapacityreach suctionpressuresof350mbar,correspondingtomaximum sizes of water-?lled pores of about 10mm. If evaporation reduces the amount of water in these ordinary soils to about20%,only?neporesare?lledwithwaterandsome protozoa become inactive. Sandy soils tend to lose water rapidly by evaporation or draining by gravity. The remaining ?ne pores may be too small, and hold water too tenaciously, to allow protozoan activity. In aquatic environments, water salinity is one of the major factors determining the range and composition of protozoan species. Stenohaline species are adapted to rather narrow salinityrangeswhereaseuryhalinespeciestolerateamuch broader range of salinities. Marine species dwelling in coastalwatersaretypicallymoretolerantof variationsin salinity than those adapted to open ocean environments. Some coastal species adjust rapidly to changing osmotic properties of the surrounding water by varying intracel- lularconcentrationsofosmolytessuchasaminoacidsand othersmallorganiccompounds. Temperature In addition to available moisture, temperature is a major factordeterminingspeciescompositionanddistributionin space and time. Cryophilic species, adapted to low temperature environments, have been identi?ed in extre- mely cold environments, including polar habitats and abyssal depths of the oceans. Thermophiles occur in shallow bodies of water receiving intense solar illumina- tion, and in thermal springs. Shallow ponds in temperate latitudessustainsubstantialpopulationsofthermotolerant protozoan species. For example, free-living thermotoler- antamoebae(capableofgrowthat37?458C)isolatedfrom surfacewaterinashallowpondinthePiedmontregionof Protozoan Ecology 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net SouthCarolina,USAincludedNaegleria(64.4%),Vahlk- amp?a(17.8%),Acanthamoeba(13.3%)andHartmannella (4.4%),expressedaspercentageoftotalabundances(Kyle andNoblet,1986).Aquaticamoebaeintemperateclimates vary in abundance seasonally. Peakabundances occur typically in spring and autumn (e.g. Anderson and Rogerson, 1995). A threshold temperature of c.108C seems to be critical for a rapid increase in population densities. Growth is diminished at temperatures below 108C.Lowdensitiesoccurinlateautumnandwinterwhen the water temperature falls below 108C. This may be attributed to low metabolic rate of the amoebae and a diminishedavailabilityofbacteriaprey.Ontheotherhand, many protozoa thrive in Antarctic and Arctic conditions where temperatures of seawater remain below 48C. Some marineAntarcticamoebaehaverecentlybeenshowntobe capable of growth at228C. Laboratory studies of temperature tolerance in the ciliateTetrahymenapyrifor- mis,typicallyfoundintemperateenvironments,showthat growthisdiminishedattemperaturesbelow108C.Growth is also inhibited at temperatures above 258C. The culture dies within a weekat a temperature of 32.5 8C(Figure 2). Furtherstudiesareneededontemperaturetolerancesand optimalgrowthconditionsofmajorprotozoanspecies. Nutrients Protozoautilizeabroadrangeofdissolvedinorganicand organicnutrients,includinginorganicsolutes(potassium, chloride, essential metals, etc.), nitrogen compounds (nitrates, ammonium and amino acids), inorganic phos- phates and organic phosphate compounds (e.g. glycero- phosphate), short-chain alcohols (e.g. ethanol) and small organic acids, including acetate, pyruvate and lactate. Theseorganicacidssometimesaccumulateintheenviron- mentaswasteproductsofmetabolismbyotherorganisms. Many photosynthetic species of protozoa require only inorganic nutrients to support photosynthesis, but they also can utilize organic compounds in heterotrophic nutrition. The so-called acetate ?agellates (including euglenidsandsomechrysomonads)areespeciallycapable ofusingshort-chainorganicacidsasacarbonsourceand subsist in relatively low pH environments. Some species require exogenous sources of vitamins (e.g. vitamin B 12 ) and have been used in bioassaysto detect the presence of thevitamins. Biotic factors Interactionsamongbiotaaresigni?cantindeterminingthe abundance and diversity of species in ecosystems. Proto- zoa, as with other forms of life, exhibit complex interac- tions within communities of interdependent organisms. Amongotherfactors,resourceavailability,photosynthetic productivity, competition for space and resources, pre- dator?preyrelations,nichespecializationandavarietyof mutual supportive/inhibitory mechanisms (including re- leaseofvitamins, growthfactorsandexudatesthateither enhance or decrease environmental quality) dynamically in?uence the abundance, diversity and stability of proto- zoancommunities. Roles in Ecosystems Protozoan communities can be categorized according to theplanofHausman(1917)into?veenvironmentaltypes based on the ecosystem where they occur (e.g. Anderson, 1988,p.141).Type1(marshpools)withwarmwaterand abundant decaying vegetable matter emitting a swampy odourcontainbacterialpredators(includingSaccamoeba limax,Di?ugiaacuminata, ?agellates such asOikomonas spp. and ciliatesColeps,Carchesium,Stylonichia,Stentor and Vorticella). Type 2 environments (clear cold-water habitatslackingplantgrowth)aredominatedby?agellates (e.g. Astasia) and some lesser numbers of ciliates (Colpi- dium and Paramecium). Type 3 environments (clear, ?owingwaterwithabundantplantlife)containspeciesof Amoeba, ciliates (e.g. Chilodon, Colpidium and Colpoda) and?agellates(Monas,Chilomonas),andtestateamoebae. Type 4 habitats (clear, small pools with abundant decomposingorganicsediments)contain?lamentousalgal growth and are rich in ciliates and ?agellates. The major genera include ciliatesChilodon,Coleps,Paramecium, the ?agellateMonas,andtestateamoebae(e.g.Di?ugia).Type 5 environments (warm-water pools with abundant algae) are especially driven by photosynthetic activity and are dominated by ?agellates (e.g. Chlamydomonas, Euglena, Monas,Synura,andPeridinium).Therearelessernumbers 3.0 0 014 Log number of cells cm ?3 Time (days) 4.0 2812 2.0 610 32.5°C 25°C 10°C 8.5°C Figure 2 The effect of temperature on the population density of Tetrahymena pyriformis. Growth is best at 258C, with a minimum temperature of 108C. Adapted from Sleigh M (1989) Protozoa and other Protists, p. 260. London: Edward Arnold. Protozoan Ecology 3ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net of ciliates (Colpoda, Campyla, Frontonia and Vorticella), heliozoa and occasional testate amoebae. Protozoa are excellent indicators of environmental health or pollution, as they are single-celled organisms living in intimate relationship to their surroundings (e.g. Foissner, 1987). They are often used as bioindicators of environmental pollution.Theyarealsosigni?cantinwaterpuri?cationin sewage treatment plants, where they help to remove organic wastes and reduce mineral nutrient load in the waterbeforeitisdischarged. Aquatic, photosynthesis-based communities A general model of a photosynthesis-based protozoan communityisshownin Figure 3.Algae,cyanobacteriaand photosynthetic?agellatesareprimaryproducersproviding a major source of carbon compounds and energy in protozoanfoodwebs.Bacteriautilizeorganiccompounds releasedintotheenvironmentbyprimaryproducers,orby deathanddecayofotherbiota,toformamajorparticulate foodsourceforsmallandintermediate-sizedheterotrophic protozoa. Bacterial predators include small amoebae, ciliatesandsome?agellates.Duringbacterialfeedingand waste egestion, minerals and other nutrients are released into the environment, thus enhancing the availability of resources for other biota, including plants. In aquatic environments, the dynamic relationships among bacteria andprotozoanbacterialfeeders,resultinginreplenishment of available nutrient resources, are an important compo- nentofwhathasbeentermedthe?microbialloop?model. Some of the resources bound up in bacterial particulates are released by protozoan predators, thus making them available for primary producers and increasing primary productivity(Figure 3).Thisenhancedprimaryproductiv- ity further fuels bacterial and protozoan growth, thus maintaining a vigorous and active protozoan/bacterial community. Some larger protozoa, including amoebae, ciliates and phagotrophic ?agellates, consume algae and small photosynthetic ?agellates. These are primary con- sumers and serve a role similar to herbivores in macro- organismic communities. Generally, ciliate abundance is positivelycorrelatedwithchlorophyllaconcentrationsor with ?agellate prey abundances in temperate freshwater lakes, further exemplifying the trophic relation between primary producers (represented by chlorophyllaconcen- tration)andciliatesasconsumers(Laybourn-Parry,1992). Secondary consumers include a wide range of larger amoebae, ?agellates (e.g. heterotrophic dino?agellates, some phagotrophic euglenids, chrysomonads, and other largeheterotrophic?agellates)andsomeciliates.Thelatter includeraptorialciliatesthatactivelypursueotherciliates and, through a variety of attackmechanisms, snare and subdue them before ingestion. Flagellates exhibit a range offeedingstrategiesencompassingosmotrophy(absorbing dissolvedorganiccompounds)tophagotrophy(engul?ng particulatefoodindigestivevacuoles).Inthesimplestform ofphagotrophy,particlesoffoodattachedtothesurfaceof thecellmembranebecomeenclosedinacup-likeinvagina- tionandeventuallyaresurroundedbyandenclosedwithin an intracellular digestive vacuole. Some species have an elaborateingestionapparatusincludingagulletorfeeding pouch with a specialized region where a food vacuole is formed. Some of these phagotrophic species, such as the euglenid Peranema spp., are capable of ingesting other euglenids nearly as large as themselves. Many amoebae snare prey by enclosing the food particle within a food vacuoleformedbythe?owingactionofpseudopodiathat graduallyencloseandengulftheprey.Largermembersof theamoebae(e.g.Amoebaproteus)arecapableofattacking and ingesting other protozoa, including ciliates. Others prey on ?agellates or algae (e.g. diatoms). Ciliate species use a wide range of feeding mechanisms, including a feeding groove where beating cilia sweep prey particles (e.g.bacteriaandsmallalgae)intoanoralpouch,wherea foodvacuoleisformed(e.g.Parameciumspp.),oranoral poreandfunnel-likecyrtos(conicalarrayofmicrotubular rods)withinthecytoplasmusedtoingeststrandsofalgae orcyanobacteria(Nassulaspp.).Somecarnivorousciliates haveahighlycomplexfeedingapparatus,suchasagaping anteriororalgroovetoencloseprey(Bursariatruncatella), anelongated?exibleprobosciswithbarbsusedtostrikeat and impale motile prey (Dileptus anser), or a conical anteriorregionwithextrusiblebarbsusedtoimpaleciliate prey and, by inversion of the cone, ingest it (Didinium nasutum). Terrestrial communities Terrestrial protozoa include heterotrophic ?agellates, amoebae and ciliates (Darbyshire, 1994). Food webs are largely bacterial-based and productivity depends on the Algae and photosynthetic flagellates Nonphotosynthetic flagellates Mineral nutrients Ciliates, raptors Ciliates Amoebae FungiBacteria Figure 3 A photosynthesis-based protozoan food web. Green arrows show dissolved nutrient flow and orange and blue arrows indicate prey and predator relations. Feeding activity of protozoa mineralizes nutrients that are available for primary production (recursive arrows). Protozoan Ecology 4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net abundance and suitability of bacteria as prey (Figure 4). Largerprotozoandensitieshavebeenfoundnearrootsof plants compared with in the surrounding bulksoil (up to tenfold higher), probably due to increased bacterial prey sustained byorganiccompoundsreleased fromthe roots. Current evidence indicates that increased protozoan grazing activity also promotes mineralization of essential nutrients in the vicinity of the roots and enhances plant growth.Ithasbeenestimatedthatinagrowingseasonas much as 25kg of nitrogen per hectare can be released for plant utilization by protozoan grazing activity. In short grassprairies,protozoaconsume1.6gnitrogenpersquare metre annually and excrete 1.2g inorganic nitrogen and 90mg organic nitrogen (as faeces). The vast majority (98%)ofnitrogenmineralizedbyprotozoaistheresultof amoebaeratherthan?agellates,oneofthemostabundant soil protozoa (Darbyshire, 1994, p. 80). Terrestrial protozoa are therefore increasingly recognized as enhan- cingsoilfertilityandplantproductivity.Protozoaarealso major components of terrestrial invertebrate food webs and serve as prey for nematodes that are consumed by microarthropods(Figure 4). Specialized Habitats Marine taxa of protozoa are distinct from freshwater aquaticandterrestrialprotozoa.Furthermore,character- isticmarinespeciesoccuramongdi?erenthabitatssuchas marshes, sandy shores, benthic locations and the water column. Each group has specialized adaptations to enhance survival within a particular habitat. Coastal, sand-dwelling ciliates, and those living along the margins oflakes,aretypicallyelongateandslender,thusimproving theirmovementamongthe?nesedimentspaces(Fenchel, 1987, p. 121; Finlay etal., 1988, Patterson etal., 1989). Some species of Remanella, Tracheloraphis, Geleia and Helicoprorodon are found only within marine sediments. Hypotrichs with somewhat ?attened bodies and ventral tufts of cilia (cirri) move with a crawling motion through the sediment particles. Testate amoebae often have ?attened tests with marginal ?anges or ?ared terminal apertures. This may help to anchor them within the sand and prevent detachment during water movement. Plank- tonic species have evolved mechanisms for ?otation and capture of prey while carried within water currents. For example, some planktonic foraminifera and radiolaria have a frothy external cytoplasm and abundant lipid reserves that aid ?otation. Long spines and radiating pseudopodiaincreasesurfaceareaandenhancecaptureof preysuspendedinthewatercolumn. Manyspeciesfoundinfreshwaterenvironmentsarealso found in terrestrial habitats. This is probably due to similarities in osmotic properties of water in soils and freshwaterhabitats.Moreover,cystsoffreshwaterspecies are undoubtedly blown backand forth by wind between soil and freshwater habitats, especially during periods of extendeddrought. Competition, niche differentiation and coexistence Resources are limited in natural environments and theoretically a species that is most competitive would eventually dominate. However, competition may be reduced when protozoa occupy di?erent niches (di?er- entiationbasedonkindoffood,locationinhabited,season for peakactivity, etc.). For example, some protozoa feed on suspended food particles, whereas others graze on particlesattachedtosurfaces.Di?erencesinkindsofprey alsoallowprotozoanspeciestocoexistinthesamehabitat. Planktonic foraminifera and radiolaria coexist within the sameopenoceanwatermass.Radiolariatendtoconsume more phytoplankton prey, whereas planktonic foramini- fera consume more zooplankton prey, thus possibly alleviating competition through prey di?erentiation (An- derson,1988).Moreover,speciesinbothgroupsformalgal symbioses, and this additional source of photosynthetic- basednutritionmayhelptoreducecompetitionforprey.In deep, unmixed lakes, the water column is typically strati?ed much of the year, with warmer, oxygenated water near the surface and more anoxic, cooler water at greater depths. Di?erent species of protozoa occur at di?erent depths, thus avoiding direct competition for resources (e.g. Finlay et al., 1988). Furthermore, in the natural environment, food particles occur in a range of sizes, allowing for di?erent species to specialize in capturingfoodofagivensize.Forexample,fourdi?erent speciesoftheciliateRemanella(varyinginsizefrom85to 300mm) coexist in marine sediments. Each consumes a Amoebae Flagellates Nematodes Microarthropods Substrate FungiBacteria Figure 4 A terrestrial protozoan, bacterial-based food chain showing predator?prey relations. Adapted from Griffiths BS (1994) Soil nutrient flow. In: Darbyshire JF (ed.) Soil Protozoa, p. 80. Wallingford, UK: CAB International. Protozoan Ecology 5ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net di?erentsizeddiatom,thusreducinginterspeciescompeti- tion(Fenchel,1987,p.94). Seasonal di?erences in abundances due to changing optimal conditions for each species, such as temperature, oxygen concentration, pH and available moisture (corre- lated with encystment and excystment patterns), etc., reduce competition. Staggered cyclical peaks in popula- tionsofdi?erentspeciesreducesinterspeciescompetition. For example, in aquatic environments, fast growing, ?attened discoidal forms of gymnamoebae (i.e. Vannella andPlatyamoeba)alternateinabundancesthroughoutthe growing season with some slower growing forms with extendedsubpseudopodia(e.g.Acanthamoeba,Vexillifera, Thecamoeba,Rhizamoeba,etc.)(AndersonandRogerson, 1995).Examplesofalternationofabundancesofprotozoa havealsobeenreportedinfreshwaterlakesandsubtropical openoceansurfacewatersubjectedtoseasonalvariations in temperature. Variations in reproductive cycles and patternsofencystmentandexcystmentcanhelptoexplain thesevariationsintemporalpatternsofabundance. Life Cycles Asexual and sexual reproduction occur among protozoa, butonlyasexualreproductionhasbeenobservedinsome groups (e.g. most gymnamoebae). Asexual reproduction includes binary ?ssion (cell division producing two daughtercells),multiple?ssion(producingseveraldaugh- tercells)andbudding(pinchingo?ofnewcellsfromacell surface). In ?agellates, the cells divide longitudinally, typically by formation of a division cleft that progresses from the ?agellated, anterior end to the posterior end. Gymnamoebae divide symmetrically to produce two nearly equal daughter cells. Ciliates divide transversely. Thedivisionplaneisthroughtheshortaxisofthecell.In manyofthesespecies,periodsofencystmentareinterposed with periods of asexual reproduction and proliferation, givingrisetocyclicalpatternsofabundance. Sexual reproduction is highly diverse among various groups and only a few examples can be given here. Some speciesof?agellatesreproducebygametogamy,thefusion of free-swimming gametes (e.g.Chlamydomonas). Fusion ofthe?agellatedgametesyieldsazygote.Thezygotemay undergoimmediatemeiosistoformhaploiddaughtercells, thuscompletingthereproductivecycle,orarestingspore may be formed and persist during adverse conditions for sometimebeforemeioticdivision.Inthecolonial?agellate Volvox, numerous ?agellated haploid cells are intercon- nected by cytoplasmic strands and enclosed within a sphericalgelatinousenvelope.Spermpacketsareproduced in one colony and swim to the egg-containing colony, where they are released and fertilize the egg cells. The resulting zygote undergoes meiosis and gives rise to daughtercolonies.Asataxonomicnote,Chlamydomonas and Volvox are included among the algae by botanists (phycologists)asaresomeotherpigmented?agellates.To avoid this confusion, some modern taxonomists have proposed that all single-celled eukaryotic organisms, including the heterotrophic and autotrophic (photosyn- thetic)formsofprotozoa,shouldbeassignedtoakingdom calledProtista. There aremanydi?erentsexualreproductivestrategies amongciliatespeciesbuttheyallinvolveabasicplanofcell conjugation. Compatible individuals pair at the anterior end, where a porous membrane is formed. Sperm nuclei are exchanged across the porous membrane. Each sperm nucleusfertilizestheeggnucleusofthereciprocalpartner in the pair. The resulting exconjugants separate and swim away to produce additional o?spring by asexual reproduction. Someprotozoahavecomplexlifecycleswithintermedi- atestagesofhighlyvariedformandhabit.Insomecases, these stages have been misintepreted as di?erent species. This condition of polymorphism (highly varied morpho- logical forms within the same species) is widely encoun- tered among protozoa. Asexual and sexual reproductive stages are interposed in the life cycle of many protozoa, usually with many asexual stages occurring between each sexual stage. Asexual reproduction supports rapid pro- liferation during favourable environmental conditions. Sexual reproduction allows for genetic variation, giving risetonewgenecombinationsino?springandenhancing survival when environmental variations may require adaptive responses. These reproductive strategies, com- binedwithacapacitytoformcystsandrestingstages,allow protozoatoinhabitdiverseenvironmentsandtoadapttoa widerangeofhabitats.Somespeciesarecosmopolitanand are found worldwide. Their cysts are carried by water currents and wind to distant locations, and they are undoubtedly transported by waterfowl and other aquatic animals as they migrate from one location to another. Protozoa,thoughamongthesmallestoflifeforms,exhibit remarkablycomplexbehaviouralandphysiologicaladap- tationsthathaveallowedthemtoinvadeandproliferatein widelydiversehabitats.Theirbiodiversity(whichincludes tens of thousands of extant species), essential role in maintainingfoodwebsandenhancingecosystemproduc- tivity,andincreasingevidenceofnumericalabundanceand diversity in widely divergent habitats worldwide give evidenceoftheirimportanceonaglobalscale. References AlbouvetteC,CouteauxMM,OldKMetal.(1981)Leprotozoairesdu sol: aspects e´cologiques et me´thodologiques. Annals of Biology 20: 255?303. Anderson OR (1988)ComparativeProtozoology:Ecology,Physiology, LifeHistory.Heidelberg:Springer. AndersonORandRogersonA(1995)Annualabundancesandgrowth potential of gymnamoebae in the Hudson Estuary with comparative Protozoan Ecology 6 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net data from the Firth of Clyde. EuropeanJournalofProtistology 31: 223?233. DarbyshireJF(1976)E?ectofwatersuctionsonthegrowthinsoilofthe ciliate Colpda steini and the bacterium Azotobacter chroococcum. JournalofSoilScience27:369?376. Darbyshire JF (ed.) (1994) Soil Protozoa. Wallingford, UK: CAB International. DarbyshireJF,AndersonORandRogersonA(1996)Protozoa.In:Hall GS(ed.)MethodsfortheExaminationofOrganismalDiversityinSoils andSediments,pp.79?90.Wallingford,UK:CABInternational. Fenchel T (1987) Ecology of Protozoa: The Biology of Free-Living PhagotrophicProtists.Madison,Wisconsin:ScienceTech. Finlay BJ, Berninger U-G, Clarke KJ,etal. (1988) On the abundance anddistributionofprotozoaandtheirfoodinaproductivefreshwater pond.EuropeanJournalofProtistology23:205?217. Foissner W (1987) Soil protozoa: fundamental problems, ecological signi?cance,adaptationsinciliatesandtestaceans,bioindicatorsand guidetotheliterature.In:CorlissJoandPattersonDJ(eds)Progressin Protistology,vol.2,pp.69?212.Bristol:Biopress. HausmanLA(1917)Observationsontheecologyofprotozoa.American Naturalist51:157?172. KyleDEandNobletGP(1986)Seasonaldistributionoftheremotolerant free-living amoebae. I. Willard?s Pond. JournalofProtozoology 33: 422?434. Laybourn-Parry J (1992) Protozoan Plankton Ecology. London: ChapmanandHall. Patterson DJ, Larsen J and Corliss JO (1989) The ecology of heterotrophic ?agellates and cliates living in marine sediments. In: PattersonDJandCorlissJO(eds)ProgressinProtistology,vol.3,pp. 185?277.Bristol:Biopress. Further Reading AndersonOR(1983)Radiolaria.NewYork:Springer. Capriulo GM (ed.) (1990) Ecology of Marine Protozoa. New York: OxfordUniversityPress. ElliottAM(1973)BiologyofTetrahymena.Stroudsburg,Pennsylvania: Dowden,HutchinsonandRoss,Inc. Fenchel T (1987) Ecology of Protozoa: The Biology of Free-living PhagotrophicProtists.Berlin:Springer. Go? LJ (ed.) (1983) Algal Symbiosis: A Continuum of Interaction Strategies.Cambridge:CambridgeUniversityPress. HemlebenCH,SpindlerMandAndersonOR(1989)ModernPlanktonic Foraminifera.NewYork:Springer. Margulis L, Corliss JO, Melkonian M and Chiapman DJ (eds) (1990) HandbookofProtoctista.Boston,MA:JonesandBartlett. Protozoan Ecology 7ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net A1929 1..7