Competition Studies of Marine Macroalgae in Laboratory Culture
Total Page：16
File Type：pdf, Size：1020Kb
/ 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). Fletcher 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.<ia (Gracilariaceae) (joties 1956). fpalens derived frotn a sitigle cvstocarp (Plate II, Fig. The fornuitioti of secotidary pit contirctioiis be- 1): gatnetophytic basal discs of clonal Gymnogongrus 'weeti basal discs of coalesced' red algal sporelings <lri'onien.\ts. The cells linked by secotidarv pit con- ;>nd confluent crusts is probably far tnoif cotiinioti- nections between individual holdfast discs of Gym- Placc- than appreciated iti tlu- lifeiaturc-. Primary pit tiogoiigriis spp. ganic-tophytes (Plate II, Fig. 1) are '•"'itieclions litiking kindic-d cells are chaiacteri.stic hotnokaryotic, coiitaitiitig getieticallv identical nu- 'ms' ^''''''^^'''ophycidae (see Pueschel and Cole clei. Secotidatv p'n cotniections were also formed - 82). Sfcouclaiy pit connections are fotind iti a between genetically differetit, although sibling, ga- great diversity of red algae fVotn many floricleophv- metophytic discs of Phxllophora traillii grown f^"rom <^ean orders. In most species, secondary pit cotinrc- meiotic tettaspotes (see Maggs 1989): the.se resulted ttons develop by ihe uneciual divisionOf an inter- in heteiokaiyotic cells (Plate 11, Fig. 2). Ihis raises ca at y a^ll lo produce a nucleate conjutictor cell that the possibility that coalescetice between genetically fuses with a neighboritig cell. This results in a tini- difTeient individuals cotild result in chimeric mul- nucleate and a biiiuc leate cell linked by a secondary tiaxial axes with filaments of two getiotypes. If co- 20 CHRIS flNE A. MAGGS AND DONALD P. ClfFNFY III. Ftcs. 1-3 Spore-hug coalescetice sec^uence fx-tween germinatitig ganic-t<>|)hylc-s