/ Phycol. 26, 18-24 (1990)
MINIREVIEW
COMPETITION STUDIES OF MARINE MACROALGAE IN LABORATORY CULTURE
Christine A. Maggs Departmetit of Biology, Queen's University of Belfast, Belfast, Northerti Ireland BT7 INN and Donald P. Cheney* Biology Department, Northeastern University, Be)ston, Massachusetts 021 15
Competition for space between different species ever, comes from spore culture studies whose ob- of benthic marine algae or between marine algae jectives were mainly taxonomic or developmetital. and encrusting animals has been primarily examined Nevertheless, these provide considerable insight itito in the field (e.g. Dayton 1971, 1975, Kooistra et al, macroalgal intraspecific interactiotis. Most past work, 1989, Paine 1990). Few studies have been conducted as well as otir own, was conducted on red algae. The in laboratory culture, although such an approach examples we will discuss exhibit several life history can provide several advantages. This paper is in- types, which cati be sutnmari/ed as follows (for ftir- tended to review observations from culture studies ther details see West and Homtnersand 1981): 1) by ourselves and others on the general topic of mac- isomorphic, iti which haploid atid diploid spores re- roalgal competition and interaction. By bringing to- sultitig from meiosis and fertilizatioti, respectively, gether a diversity of observations from macroalgal grow itito trtorphologic ally similar gatnetophytic atul culture studies, we hope this brief review will stim- tetrasporophytic thalli that may be entirely crustcjse ulate their greater u.se to test ecological thecjry on or form erect axes from a crustose holdfast (e.g. ccjmpetition. In particular, we will describe the in- Chondrus, Graciiaria): 2) hetc-romorphic, in which teracticjns that occur when fleshy algal crusts, crus- only the haplcjid, gatnetophytic phase develcjps erect tose holdfasts, or sporelings of the same c)r different axes, atid the diploid tetrasporophyte is crustose (e.g. species grow together. Since these morphologies are Gymnogongrus ?f)atens, Phyllophora traillii); 3) Rliodo- restricted to two-dimensional growth, observations physema-typf. in which crusts are haploid and dip- in laboratory culture allow for easy macro- and mi- loidi/ed carpogotiia divide into tetrasporocytes atid croscopic examination of interaction between indi- regetierative tetrasporatigial stalk cells (e.g. Rhodo- viduals (Pentecost 1980) and estimation of ccjmpet- phy.iema elegans, see Satuiclers et al, 1989), itive success by measurements of areas occupied (Dale The ability of sporelittgs atid crusts of a sitigle 1985). species to grow together atul fortn completely co- Culture techniques were first applied to dedicated alesced masses has been described in several studies investigations of competition between species of ma- of erect atid crustose, fleshy and corallitie red algae. rine algae by Russell and Fielding (1974) and Fletch- We propose here that observations of these phe- er (1975). Russell and Fielding examined interspe- nometia ittdicate that cooperatioti, rather thati com- cific competition among a brown, a red and a green pc'titioti, is the tnost sigtiificant feature of intraspe- filamentous algal species {Ectocarpus siliculosus, Eyth- cific interactiotis of this type. We suggest that the rotrichia carnea and Ulothrix fiacca).Fletche r worked benefits of growitig as completely coalesced groups with a brown crustcjse alga {Ralfsia spongiocarpa) and of crusts cjr platits with crustose holdfasts outweigh twcj red crusts {Porphyrodiscus simulans and Rhodo- the costs associated with crowding. The formatioti physerna elegans). Both studies reported evidence of of intercellular connectiotis fjetween contiguous in- interspecific inhibition. Fletcher suggested that the dividuals is central to the ability to cooperate. production of antibiotic compounds (allelopathy) by Ralfsia enabled it to inhibit the growth of the two .Sporeling CoalesceJice red algal cru.sts. Antibiotic compounds have also been The most detailed observations to date on spore- implicated in the inhibition of benthic diatom growth litig coalescetice are of the red alga Chondrus crispus in ctikures of crustose germlings af Chondrus crispus (Gigartinaceae), which has an i.somorphic life history (Khfaji and Boney 1979) and may be involved in the involving the formatioti of erect fnjtids frotn basal suppression of cyanobacteria by the red crust Peys- discs of sporelitigs of both phases. The coalescence sonrielia immersa (Maggs, unpubl.). of basal discs of sporelings of each phase has been The principal contribution of culture studies to described by several atithors iticluding Rosenvinge our understanding of macroalgal cc^mpetition, how- (1931), Tveter and Mathieson (1976), Chen and Taylor (1976) and Tveter-Gallagher and Mathiesoti ' Address for reprint requests. (1980). Based oti light (Tveter atid Mathieson 1976) 18 MACROALGAL COMPETTTION IN l.ABORA TORY CULTURE 19
I'l.AtK, II. Ktc.s. 1-4. Se-cond:it) pit coniic-c tions and cell fusions formed between cells of two crustose algal lndtviduals when crust "latgins come into contact. Arrows show dire-ction of growth of each individual; arrowheads indicate cell fusions or secondarv P'pitt oniiectiotis betwc-eti cc-lls ot cliflc-ient th.illi. Scale- bars = 20 tim. Ftc. 1. Gwinogoiigriis tpatens. Secotularv pit connections between cells vvo ge-iu-ticiilly icic-iitit al diploid c rusts grown Irom spores of a single cystocarp. Mativ secondarv pit contiections cKcur between cells «itliin a tluilliis ,md ic-sult in iiiultinuc le.ite- cells. Ft<;. 2, Phytlophora traitlii. Secondary pit connections between cells of geneticallv < itlc-rciK sililiiig basal discs gruuti Irom meiotic tetraspores of a single parent. FtG. 3. Gtow.':tphonia capittans. .^butidant cell fusions oiiiic-d along du- line of junction between two ge-ne-tieallv idetitical crusts derived fVoni tnitotic bispores. FtG. 4. Rhodophysema rtegans. v.cll lusions between two genetically diffc-rent crusts grown ftom meiotic tetraspores.
;nul electron tnicnxscope(Tveter-Gallagher and Ma- pit connectioti (Goff atid Coleman 1986, Pueschel thieson 1980) ob.servatiotis, coalesc c-tue in Chondrus 1988). Botli nuclei persist in binucleate cells btu, as has been cliatac teri/ed as exhibiting the followitig far as we know, there is no evidetice as to whether leatures: vertical atul hori/ontal alignment of cells, one or both titiclei participate iti cellular control. ( uticular contituiity, atid fortiiation of secotulaty pit Meristetnatic dividitig cells do not normally become totitiections between cells of confluent itulividual bitiucleate or nuiltiiuuieate. Some parasitic red al- spotelings. Otuc- two or tiiore sporc-litigs have co- gae form secondary pit connections with host cells ale.scc-d, thc-y may bc-conie indistinguishable. Occa- (Goff and Coletnati 1985). siotially, however, a furrow is left along the junction As yet, very little is known about what effect, if between itidividuals due to cellular damage during am, getietic sitnilaritv and ploicU le\el have upon coalescetu:e. The- degiee of datnage appears to be coalescence and formatioti of secotidarv pit contiec- lelated to the stage- oidc-M-loptiu-nt of the sporelings tiotis. We ha\e exatnitied several members of the at the iiiii(> ol coalescetice, with less damage occtn- Phyllophoraceae with a view to detectitig the effect '•"iR tn vounger platits (1 vetet-Gallagher and Ma- of getietic relatiotiships on the formation c^f second- thteson 1980). SitiiilarcoalesccMiceoi sporelings also ary pit connections betweeti individuals. Secondary has been teportecl in the- red algae- Mastocarpus (as pit cotitiec tions were obsetved betweeti the follow- '"^'•"'"""") stellatus (Petrocelidaceae) (Tveter and ing geneticallv idetitical itidividuals grown from mi- Mathieson 1976, Rueness 1978) and Grncilnria ver- tospores: tetrasporophytic crusts of Gymnogongrus ruco.
III. Ftcs. 1-3 Spore-hug coalescetice sec^uence fx-tween germinatitig ganic-t<>|)hylc-s pioducc-el frnni sibling tetrasporc-s of Chnndru\, ,,. , crispus.,.,., Coalesceti,,,.encc e is occurring at an early developmental stage. Sporelings have be-e-n staine-el with neutral te-d. Ftc;. I. Initiation of coaleseetue fn-tween thre-e spore-lings. Note that the top two sporelings are- still cic-arly sc-patale-d by cuticdiar tnaterial (ct) after adheretice whereas at a slightly later stage, the cuticular material and side iiulentation are tnuch rc-ducc-d as coale-scence (c) is initiated between the middle and bottcjm sporelings. Seale bar = 25 ^m. FtCi. 2. Intertne-diate stage in coalescence. Note the nearly complete coale-scence of cells and the small cuticular inde-ntatioti (arrow) that remains at the juiutioti between the original sp.ireliiigs. Siale liar = 25 ^m. Ftc. 3. Final stage- ui coalescc-nc e, iti which the original sporelings have cotnpletely coalc-sc e-el at the jiiiK tiiiii l>e-twe-e-ii them (arre)w) and are no longer elistitiguishaljlc (i,c-. they appear as a single- ce-ll mass). Scale bar = 30 ^m.
alescence occurred between haploid atul diploid opmental stage is illustratc-d iti Plate- III, I'igures 1- holdfasts, such a chimera could jirovidc- an addi- ?i. 1 lu- nc-t rc-sult in stich cases is cc)iiiplete coales- tional tnechanism for mixecl-[)hasc- rc-produc tion iti cc-ti('<- ol tlu- otiginal s|)ot(-litigs; th;it is, secotulaty single thalli besides those described by van der Meer pit cotinec tiotis are ptctchic c-d lx-twc-c-n tlu-ir cc-lls, and Todd (1977) and Oliveira and Plastino (1984). atid they become virtually itidistitiguishable (Plate However, when diploid crttsts and haploid basal discs III, Fig. ?i). Sitnilar results were- obtained for red oi Gymnogongrus fpatens were grown together, sec- and grc-c-ii-pig:iu-iitc-(l (i.e. tion-siblitig) spore-ling co- ondary pit connections were not formed bc-tween alesccMue, when coalescc-nce occuiic-tl at an early individuals of different ploidy. Instead, the thallus developmetital stage (("hc-tiey, unpubl). margitis grew utidc-r or over eac h other. These ob- When sibling sporelings coalesced after eac h was servations suggest that incompatihilitv rric-c hatiistns already well developed, thc-y rc-tnainecl as distitict may discriminate between individuals of different c-tititic-s with c Ic-ar tnatginal clist itic I lotis oi Itiitows ploidy although not between siblitigs of the same separating them (Plate- I, Fig. 2). Sitnilar tnargitial plc)idy. fiirrows also oc c iirrecl in t he few e ase's of c c)ale"se e-iu e- Ititraspecific coalescence between sporelings of we obsc'rve-d hc-twe-e-n s|)e)re-litigs of difTe're-tit ploidy similar and different ploidy level has been investi- le-vc-1 (i.e-. betwec-n gree-n gatiie-tc)|)ln tie and ic-ci te-t- gated by us in Chondrus crispus ancl Gracilaria spec ies rasporophytie basal elisc s), t c-gat ellc-ss ol whether the usitig ptgtnetitation markers to distitiguish dissitnilar spore-litigs coalesced early or late- iti developmetit individtials. In Choudriis crispus, coalc-sc c-tue- was c-x- (i'hitc- I, I'ig. '.^). itite-re-stingK, the- arc-a ol the- ic-d, aniined between green-pignientc-d gatnc-tophytic te-tiaspoiophytic basal disc was always gte-ater than sporelings produced from tetraspores of a green mu- that of the greeti, gatnet<)|)liytic disc, which it |)ar- tant and red-pigmt-ntc-d ganu-tophytic or tetrasporo- t ially sttrre)ttnelc-cl. Whethc-t this was cause-el by tlu- phytic s|)orelings, prodticed from tetrasjjores atul c ulttitc- cotulitiotis (e.g. irradiance levels) or reflect- carpospores, respectively, of red, wild-ty})e platits. e'd itihc-ic'tit ploidy diflrie-iH e-s is unknown. Ihilot- Our results for coalescence betweeti sporelings of tiitiate-ly, it was tieit dett-t tiiitie-el whe-the-t se-eotulaty the same ploidy level were similar to those of Iveter pit cotitie-c tions were produced by platits either with- atul Mathieson (1976), whether the sporc-litigs were iti or l)e-twe-e-n ploidy le-ve-ls in eases where- individtial produced by sibling spores (i.e. catnc- from the- same spore-liiigs i e-tiiaiiie-el distinct. Otir rc-sults lor eo- parent) or not. Ihe tvpical secjuence of coalescence alescc'ticc- bc-twe-eti spote-liiigs ol the- same- plc)iclv lc-vc-l for sibling sporelitigs coalescing at an early devel- we-re- thus similar tc) thc)se- e)f I vctc-t and Mathie-soii MACROAt.GAt. COMPETITION IN LABORATORY CULTURE 21
(1976), whether the speires were similar in getiotype genotnic hybrid that has a single nucleus per cell, (i,e. catne fteitn the satne patent) e)r tu)t. but in these utiinduced ftisions, the nuclei of both Sitnilar spotelitig coalescence experiments have cells pet sist and usually remain in their original po- been conducted with Gracilaria. both withiti atid be- sit iotis. There is no evidence as to whether the cy- tweeti different species (Cheney, unpubl.. Duke and toplasm and other organelles of the originally sep- Cheney, utipubl.). 1 hat is, we exatnitied coalescence arate cells tnix or retnain separate. The frequency between gteeti- atul red-pigmetited gatnetophytic of fused cells along the junction between crusts was sporelings produced from tetraspores of green mu- greater than that between filaments of the same crust tant (NMG; van der Meer 1986) and red, wild-type (Plate II, Fig. 3). Since the cultures were all clones, Gracilaria tikx'ahiae plants, as well as between green- the ftised cells were hotnokaryons. Cell fusions were pigmetited gatnetophytic G. tikvahiae speirelitigs f re)m also observed between individuals in tetrasporangial NMG and red-pigmented G. chilensis sporelitigs pro- cultures oiR. elegans (Plate II, Fig. 4). These meiot- duced from tetraspores of a red, wild-type plant, lti ically derived crusts (Saunders et al, 1989) are ge- both types e)f co-cultute experimetits (i.e. intta- and netically different, and fu.sed cells of different in- interspecific), spoteling coalescence was achieved, dividuals are therefore heterokaryeitis. atid red and green, bicoloted cell masses were pro- Iti ceititrast to the somatic cell fusions described duced (Plate I, Figs. 4, 5). Whether the ted and above, efforts to fuse spores of Gracilaria have prov- green sporelings were of the same or different species eti unsuccessful (Duke and Cheney, utipubl). Even appatently dicl not affcn t their capability to coalesce with polyethylene glycol (PFG), which has been used atul even te) form secondary pit contiections (Plate for itising protoplasts (Cheney 1990), we were un- I, Fig. 5), as long as coalescence occurred at an early able to fu.se spores of any ploidy or strain. This fail- developmental stage. Otie or beith cell types within ure appears to be due to the presence of cell wall the bicoleited cell tnass stibsc-ejuetitly ptodtued up- tnaterial, sitice wall-less ptotoplasts of Gracilaria tik- 'ight fre)tuls that were always of the same pigmeti- 'vahiiic and G. chilensis have been successfullv fused tiition as the cells that pioduced them. Although (Cheney 1990), Chondrus crispus spores did not fuse both red- and greeti- pigtiietited frotids were pro- either, even in the presence of PEG, but PEG pro- duced from a single bicolored cell mass, individual tnoted spore adheretice atid thtis the formation of chimeric fronds were tiot observed. 1 he ability for coalesced sporelitigs. sporelings of two non-interfertile species (i.e. G. /;A'- vahiae and G. chilensis. Cheney and Bradley, utipubl.) Ecological and Evolutionary Implications to coalesce catne as a stn-prise to us, atid raises sotne Much of the information presented here is pre- interesting citiestie)tisabe)tit self-self recognition. How liniitiary btit it poitits to the overwhelming conclu- coinnie)iiplace this phetu)nietie)ti is withiti the getuis sion that coalescence and intercelltilar contact be- Oracilaria or other algae needs tei be examined. tween individuals are far tnore widespread in red algae with crustose thalli or sporeling stages than is Somatic Cell Fusions generallv tecogtii/.ed. Fxcept for the studies of Jones Cell fusie)ti differs frotn the situatieiti de.scribed (1956), Tveter and Mathieson (1976) and Tveter- above in that thete is a ditcxt cotitact between the Gallagher and Mathiesoti (1980), these phenotnena cytejplasni e)f the cells inveilved witlunit the fortna- have received little attention to date. However, their tion of a conjututeM- cell. Direct cell fusiems occtir ecological and evolutionary consequences could be betweeii cells e)i the satne thallus in a tuttnber of signifu ant. species iticluditig metnbers of the Kallymeniaceae We propose that stich coalescence atid intercel- (Codoinier 197'V Hansen 1977), Corallinaceae (Ca- lular contact should be viewed as a mechanism for bioch 1970), atid iti Rhodoph\.scma spp. (PPaltnari- utiititig separate individuals into a single "super-or- aceae; Saunders et al, 1989), As far as we can de- ganism." There is coiitititiitv of the plasma mem- termine, naturally-occurring fusions betweeti cells brane between cells linked by pit connectiotis, both of different individuals have pteviously beeti re- pritnary and secondary, and effective ionic com- ported only for one- nieniber of the Ce)i allinaceae tniiiiicatiein occurs via pit connections (Bauman and (Afonso-Carrillo 1985). Probably fhe best ktiown Jeities 1986). Two ituiividual sporelings or crusts exatnple of sotnatic cell fusion is the work by Waa- joitied by .secemdary pit ceinnections might, there- latul and colU-agues describing the indtued fusion fore, be expected to be tinder the same metabolic betweeti vegetative cells of tnale and female strains contt ols atid to behave as a single organism. In other "f the red alga Gri(ftthsia tenuis (Ceratniaceae) (e.g. words, these phenomena suggest that intraspecific Waalatid 1978), However, we have observed uiiin- cooperatioti is occtirritig rather than competition. duced cell fusiotis between cells of adjacent crusts Coopetation may be defitied as "a dvnamic ecolog- in mitotically teprodttcing clonal ctiltures (see Maggs ical state of ot ganistns living in aggregation char- 1988) of bisporatigial Gloiosiphonia capillaris and tet- acterized by siifficietit muttial betiefit to outweigh rasporatigial Plagiospora gracilis (both Gloiosiphoti- disadvantages a.ssociated with crowding" and is usu- laceae) atul of bisporangial Rhodophysema elegnns. ally restricted to cases when there is a risk of fitness During preitoplast fusion, nuclei tnay fuse to form a lo.ss if others do not participate (see Buss 1981), We 22 CHRIS! INE A. MAGGS AND DONALD P. CHENEY think that intraspecific cooperation occurs bcjth has suggested that coalescc-cl sporelitigs tnay be more among crustose algae and those that produce up- resistant to gra/itig. Ceiale-sec'd holdfast systems could right fronds from basal discs. potentially be of c-volutiotiaty significatue in actitig In the crustose algae we examined, the fusion zone as a mechanistn analagous to a seed pool iti vasctilar between individuals shows an enhanced frequency plants (see Templeton and Levin 1979). As a result of cell fusions and secondary pit connections, which of sporeling ceialescence, such perennial holdfasts could increase mechanical resistance to damage. In couldac t asa buffer against c-litnitiation by "storitig" addition, a continuous coverage of the substratum different genotypes for future- frotul procltutieiti. The without gaps between individuals will reduce the ince)rporatie)ti e)f'less-ce)mpetilive basal discs into the ability of competing algae to gain a foothold. ceialesced supet-orgatiisni, rather thati their destruc- For species that form erect axes, there is gcwd tion by e)vergrowth, will also tetui to niaititain ge- evidence that cooperation between coale.sced indi- netic cJivc-rsity. Jones (1956) confirtned that spore- viduals is cx:curring. A tendency for erect axes to ling coalescence actually occurs in the field, and form at the junction between different holdfast discs Cheney (unpubl.) has observed gametophytic and has been observed in several red algae including spore)phytic Chondrus axes arising from the same, Mastocarpus stellatus (Rueness 1978) ancJ Ahnfeltia pli- prc-sumably ce)alesced, heildlast. Speirelitig ceiales- cata (Ahnfeltiaceae) (Maggs and Pueschel 1989). ceiice may be promoted iti Chondrus by the release Likewise, reproductive .sorus development appears of spores iti a sticky, mucilaginous plug. The devel- to be stimulated at the junction between Ahnfeltia opment of a turf of youtig axes from a coalesced fastigiata crusts (Maggs et al. 1989), Earlier initiation holdfast provides the benefits e)f a turf lifestyle such and faster growth of uprights are promoted by co- as resistance to desiccation, grazing atid mechanical alescence of sporelings in Gracilaria verruco.sa (Jones damage (Hay 1981, Carpenter 1990). 1956), Chondrus crispus and Mastocarfms stellatus Clearly, mueh tneire- infortnatie)ti is needed on (Tveter and Mathieson 1976). Jones (1956) pointed tnatiy e)f fhe aspects of ititraspc-cific ititc-ractie)ti we out that G. verruco.m grows in habitats subject to sand have metitioned, The.se itulude the tecogtiition e)f inundation, so that the rapid formation and growth relatedness as measured by fe)rmation of .secondary of fronds would be particularly advantageous. The pit eoiitiectie)ns e)r cell fusie)ns atul the perfeirmance mechanism cjf such enhanced shoot formation is un- of coalesced versus solitary itulividtials it) interspe- clear, but growth hormones have been suggested as cific competition or utider environnu-ntal stress. We a possible cause in other reports of increased algal have no evidence of the- cc)sts involved in intraspe- growth due to crowding (Mshigeni 1974). It is also cific cooperation but suggest that these could in- likely that increased erect axis development in plants clude grc-atc-r competitieiti for lintrie-tits and shading with coalesced holdfasts is related to the cessation eflects. We fee-l, he)wever, that the- apparetit regu- of lateral growth of holdfast tissue, Jones (1956) and lation of total frond numbers by a coalesced holdfast Tveter and Mathieson (1976) suggested that the to- group may be significant in minimi/itig dc-trimetital tal number of fronds formed by a coalesced group effects of ce)o[K-ratie)n. of holdfasts was reduced relative to the same num- Finally, althotigh we have c-tnphasizc-d the tc-d al- ber of uncoalesced basal discs, possibly because the ga(- iti this mini-review, we- do tujt belic-ve that the first-formed fronds suppress growth of others. Re- phenonietia we have described are unic|ue to the red moval of the initial fronds of a ccjalesced sporeling algae. Recently Aberg (1989) tepeirted that hold- group of Chondrus crispus stimulated the develop- fasts from diflerent itidividuals ol ihc- browti sea- ment of new fronds both from the same basal disc weed Ascophyllum nodosum can fuse so that what ap- and from adjacent discs. The existence of metabolic pears to be a single he)ldfast originates from tneire interaction between individuals in a coalesced group that one zygeite-; Paitie (1990) has observed apparent could be investigated further with species showing cytoplasmic ce)tititiuity betweeti haptera of acljacent photoperiodic requirements. It would be very in- Postelsia palmaeformis plants. We expee t that coales- teresting to determine whether the physiological re- cence and close cellular contact might also occur in sults of photoperiodic stimuli could be transmitted crustose browti algac- such as Ralfsia. The ability of between frcjnds of different individuals via coalesced the coenocytic greeti alga Codium lo overgrow and holdfasts. exclude- othc-r ititertidal algat- in (he fic-ld (Santelices Besides enhancing the colonization by and estab- et al. 1981) tnight be due in part to coalescence e)f lishment of a group of plants, sporeling coalescence individuals. The occurtetice- and sigtiificancr of co- also contributes to longevity by forming a large basal alescence n<-eds to be examined further iti all groups holdfast. In plants such as Chondrus crispus, the hold- of macroalgae. fast .system is perennial and provides a stable, resil- ient and long-lived source of new fronds (Taylor et t).P.C. would like to thank Arthur Mathieson for his support of al. 1981). The capability of such a holdfast to persist the Chondrns work, ("liff Dukr for help with Gracilaria studies and propagate new fronds vegetatively over a long ancl John van der Meet for green mutants of f)oth getiera. C.. A.M. time period offers a significant competitive advan- gratefully ac ktiowledge s helpdil elisc ussions with Hugh Fletcher tage over plants without such a system. Cheney (1978) and Viattfiew Dring. MACROAt.GAL COMPE TTTION IN LABORATORY CUt.TURE 23
Question (Paine-): Pe-rlormatiee could be measured, at the least, as Goff, L. J. & Coletnan, \. W. 1985. The role of secondary pit thallus mortality, reproductive output or gtowth tate. If labo- cotniections iti te-d algal parasitism.y. Phycol. 21:483-508. latory geiu-tate'el plants were outplatited to a variety of natural 1980. .\ tu)vel pattern of apical cell polyploidy, sequential (field) cotiditions, what diffetences in these factors would you polyploidy induction atid intercellular nuclear transfer in the expe-ct to observe in hotnokatyotic versus heterokaryotic plants? red alga Poty.siphonia. Am. f Bot. 73:1 109-30. Hatisen, G. I. 1977. Cirrulicarpus carotinen.sis. a tiew species in An.sxrer: We have no evidence as to the significance, c-ven in cul- the Kallytneniaceae (Rhodophyta). Occas. Pap. Farlow Herb. ture, of the fot tnat ion of hetetokaryotic cells and chimeric frotids. 12:1-22. Utitil thete is sotne utiderstatiding of the role of tnultiple tiuclei, Hay, M. E. 1981. The futictional motphology of turf-forming Iticluditig those of differetit getiotypes, tio theoretical prediction seaw-eeds: persistence in stressful marine habitats. Ecotogy 62: can be made. 739-50. Jones, W. E. 1950. Effect of spore coalescence on the early de- Question (Carpenter): Within an algal species, is there evidence velopment of Grnri/nrm xvrnicosa (Hudson) Papenfuss. Xature for more fVc-cjuent spoteling or holdfast coalescence in particular (Lond.) 178:426-7. physical or biological environments, sue h as actoss a desiccation Khfaji, .\. K. &: Boney, .\. D. 1979. Antibiotic effects of crustose gradietit or in envirotitnetits with high vetsus low gta/^er abun- germlitigs of the red alga Chondrus crispus Stackh. on benthic dance, that would give genotypes that coalesce' a phvsiological or diatoms. Ann. Bot. 43:231-2. eleterrent advatitage? Kooistra, V\'., ]oosten, .\. & van den Hoek, D. 1989. 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Chondrus holdfasts in natural populations and in culture. Pror. Dayton, P. K. 1971. Competition, disturbatice and cotnmunity Int. Seaweed Symp. 8:140-5. organization: the provision and subsecjuent utilization of space Tetiipletem, A. &.- Levin, t). 1979. Evolutionary consequences of iti a tocky ititertidal commutiity. Ecol. .Monogr. 41:351-89. seed pools. Am. Xat. 1 14:232-49. ~ 1075. Experitnetital evaluation of ecological clomitiatice Tveter. F.. Sc Mathiesoti, .\. C. 1976. Sp J. PhycoL 26, 24-30 (1990) A COMPARISON OF AIR AND WATER AS ENVIRONMENTS FOR PHOTOSYNTHESIS BY THE INTERTIDAL ALGA EUCUS SPIRALIS (PHAEOPHYTA)' Tom V. Mad.sen^ and Stephen C. Mciherly Department of Biology and Pre< linical Medicine. The Sir Harold Mitchell Building, The University. Si. Andrews Fife, United Kingdom KVlf) '.rVW ABSTRACT as the tidf level changes. When in water, the algae grow and photosynthesize in an environment with The response of phntnsynthesis and respiration of the a relatively low availability of light becau.se of re- intertidal brown alga Fucu.s spiralis L. lo light and tem- fk'ction at the water surface and attenuation within perature at ambient and elei'ated concentratioyis nf in- the water columti. Althotigh the total dissolved in- organic carbon was investigated. The light-saturated rate organic carbon (DlC) coticentration is higher in aer- of photosynthesis was greater in air at 15° C and 20° C, ated seawater, 2.3 mM compared to about 15 nM but greater in water at 10° C. Light cnmpemalion point in air, the majority of DlC is bicarbonate (HCO, ) and If, was ahout 50% lower under submerged reUttix