Daylength, Temperature and Nutrient Control of Tetrasporogenesis In

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Daylength, Temperature and Nutrient Control of Tetrasporogenesis In J. Exp. Mar. Biol. Ecol.,158 (1992) 197-217 197 O 1992 Elsevier Science Publishers BV. All rights reserved 0022-0981/92l$05.00 JEMBE 0I762 Daylength, temperature and nutrient control of tetrasporogenesisin Asparagopsisarmatq (Rhodophyta) Michael D. Guiry and Clinton J. Dawes Depaftmenl of Botany and Martin Ryan Marine Science Institute, University College Galway, National Llniversity of lreland, Galway, Ireland; Department of Biology, University of South Florida, Tampa, Florida, USA (Revision received 23 December 1991; accepted24 Jantary 1992) Abstract: The formation of tetrasporangiain Falkenbergia-phasetetrasporophytes of Asparagopsisarmata Harvey (Rhodophyta : Bonnemaisoniales)isolated from introduced populations in Ireland and Italy, and from native populations in Victoria, Australia, was examinedin temperature-controlledwater-baths at 2'C intervalsfrom 11-23 " C and aI 1- or 0.5-hdaylength intervals from 8-12 h. At a daylengthof 8 h, Irish plants formed tetrasporangia only at (15-)17(-21)'C, Italian plants at 17-21'C and Australian plants at l3-17'C. However, after an incubation period of 5 wk, only the Italian strain consistentlyshowed 100/. reproduction under these conditions. At 17'C, the critical daylengthfor tetrasporogenesisis 8-9 h for the Irish and Australian strains and 9-10 h for the Italian strain. These results indicate that all three isolates differ in their responseto environmental variables.It is likely that the Mediterranean and Irish populations thus representseparate introductions into the Northern Hemisphere and that Australia was not the source of these plants. The abundance of gametophytesof this speciesat Messina, Sicily, in April and May is explained by a reproductive "window" of daylength and temperature for tetrasporogenesisfrom mid- November to late January. In Victoria, Australia, temperaturesare inductive all year but daylength at the water surface is never < 9.5 h. However, it is considered that tidal ranges of 2-3 m cause the effective daylength in winter to fall below the inductive threshold. In northern Europe, the restricted geographical distribution of gametophytes is probably determined by tidally and/or topographically induced shorter daylengthsin late October and November, and also by higher temperaturesin the intertidal on warm days. Previously reported responsesto N and P levels in enriched seawatermedia were not confirmed and may have resulted from incubation at suboptimal temperatures.Arsenic and iodine supplementationappears to be necessaryfor reproduction only in the Irish strain. Key words: lqparagopsis armata; Control ofreproduction; Daylength and temperature effects;'Falkenbergia- phase; Introduced seaweed;Nutrient effect lNtRonucrtoN The marine red alga Asparagopsisarmeta Harvey (Bonnemaisoniaceae,Bonne- maisoniales)was endemicto the SouthernHemisphere until it was introduced into the Atlantic and the Mediterraneanin the early part of the presentcentury (Feldmann & Correspondenceaddress: M. D. Guiry, Department of Botany and Martin Ryan Marine ScienceInstitute, University College Galway, National University of Ireland, Galway, Ireland. 198 M.D.GUIRY AND C.J. DAWES Feldn.rann,1942). The spcciesis now u'idcly distributedin the easternnorth Atlantic from the British Islessouth to Senegal,including the Canaryand SalvageIslands, and possiblythe Azores(Price et al., 1986;South & Tittley, 1986),and is widespreadin the Mediterrancan, although gametophytesare regularlyfound only in the western basin. J. Feldmann& G. Feldmann(1939a,b,1941,1942) discovered that the separately described speciesFalkenbergia rufolanosa (Harvey) Schmitz was the tetrasporangial phase of Asparagopsisarmata by germinatingthe carposporesof the latter entity and obtaining plants that resembled the former. A similar life history for A. tariformis (Delile)Trevisan was establishedin culturefor plantsfrom Japanby Chihara(1961), who grew carpospores and obtained a Falkenbergia-phase,and for plants from Venezuelaby Rojas et al. (1982),who found that tetrasporogenesisoccurred at24oC, S:16h. Reproduction in the Falkenbergia-phaseof A. armata is reported to be rare and restrictedto autumn.The only publishedrecords for the British Islesare: Mclachlan (1967),rvho found fertile plants in Cornwall on the south coast of England in mid- October 1966; De Valcra etal. (1979)rvho collectedfertile plants at Finavarra,Co. Clare,Ircland, in October 1916,and Guiry et al. (1979)who reportedthat populations in Devon and Cornwall were forming tetrasporangiain November 1912. In northern France,J. Feldmann(195a, p. 94) remarkedthat plantsof Ihe Falkenbergia-phaseare not fertilein the irrea around Roscoff,but further south,in Portugaland Morocco, fertile plantsare found from Decemberto March (Gayral,1958, p. 288;Ardre, 1970,p. 143), and gametophytesare regularly found on the Atlantic coastsof Morocco (Gayral, 1958), Portugal(Ardr6, 1970),Spain (Seoane-Camba,1965) and France (Feldmann,1954). The perceivedlack ofreproductive tetrasporophytesin the British Isles and radically differentdistributional patternsofgametophytes and tetrasporophytesgave rise to early speculationthat both phasesreproduced independentlyby vegetativemeans (Dixon, 1964, 1965).De Valera & Folan (1964)further suggestedthat a decreasein the fertility of Irish gametophytesof l. ctrmcttamay have occurred in the period since its intro- duction, implying vegetativereproduction by the gametophytes,but concludedthat their materialwas not adequateto confirm this; they were also of the opinion that Irish ganretophl'ticplants r,verebecoming smallor and lessrobust. The Provisionalotlas o/ the nrurineulgueofBritainandlrelanrl(Norton, 1985,Mapsl6and 77),indicatesthatthe Folkenbergia-phaseof A. arntata is now widely distributed on western and southern coasts from Shetland to Cornwall, but the Asparagopsis-phasegametophytes are confined to restrictedareas of the west and south of Ireland. and in Britain are known only from the south-westcoast. In an attempt to establish the environmental parametersfor reproduction in the Falkenbergia-phaseof A. armata,Oza (1977,1989) grew a strain from Roscoff, Brittany (from the culture collection of H. A. von Stosch),under a range of temperature,day- lengthandnutrientconditions.Tetrasporangiawereobtainedonlyat15 t 0.5'C,6: i8 or 8 : 16 h, in media with low levels of nitrates or phosphates,and containing small amountsof As,O. and KI. Ltning ( 1981), using the samestrain, obtained reproduction TETRASPOROGENESIS IN ASPARAGOPSIS ARMATA 199 at 15'C, 8: t0h, in enrichedseawater media with low levelsof nitrate(<700prM NO.,), and found that a night-break was effectivein suppressingtetrasporangiai for- mation (confirming the photoperiodicnature of the response),but did not statewhether arsenicor iodinewere required for reproduction.Using the samestrain, Knappe (1985) carried out a more detailed study of the effectsof daylength at 15'C, quantifying the responseby countingspores. Casual monitoring of an intertidal population of t"heFalkenbergia-phase of A. armata in Galway Bay at 1- and 2-wk intervals from Septemberthrough December 1985 (Breeman & Guiry, unpubl. data) indicated that no sporangial production occurred during this period, even though severalwaves of reproduction took place at this time in the related,introduced speciesBonnemaisonia hamifera Hariot (Breeman & Guiry, 1989). As the temperature optimum for maximum reproduction in Bonnemaisonia hamiferais reportedto be 15"C (Oza,1971,1989;Liining, 1981;Knappe, 1985),this lack of reproduction in Asparagopsisarmata seemsto be in conflict with the published data. Severalqr.restions arc thlls apparentwith regardto the distribution and reproduction oC, of Asporagopsisarntattt in Europe:(1)If inductionoftetrasporangiais possible at 15 then why is reproduction so uncomnon in plants of the Falkenbergia-phasein the wild nearthe northern limit of distribution of A. armata?(2) Why aregametangial plants very confined in their geographicaldistribution near the northern limits of the speciesand to the Mediterranean even though the tetrasporophytesare more widely distributed? (3) Were Europeanpopulations of the speciesintroduced from Australiaand are they the result of a singleintroduction ? (4) What are the effectsof nitrate, phosphate,iodine and arseniclevels in enrichedseawater media at optimum temperatures? MRrpRr,qls AND METHoDS ORIGIN OF CULTURES Plants of the Falkenbergia-phaseof Asparagopsisarmata were isolated into unialgal culture using reproductivelysterile held-collected plants from the west coast of Ireland collectedon 6 February 1985 (Culture GALW 510, New Quay, Co Clare; 53'N, 09'13'W) and from Sicily,Italy, on 4 June 1987(Culture GALW 566,near Messina; 38"11'N, 15'33'E). Unialgal cultureswere obtained by continuouslyexcising the 2's apicesof rapidly growing plants at 16 C. 16:8tr. U-sprmol photons'm Carposporesfrom cystocarpicplants of A. armata collectedin the intertidal of Victoria, Australia,on 28 October 1987(Culture GALW 604, Sorrento;38'20'S, 144"45'W) wereinoculated into plasticdishes, grown at ll"C, 14: t0h,20-25pmol photons' m 2.s r, and a unialgal isolate of the Falkenbergia-phaseobtained. Cultures were subsequentlyrendered clonal by selectinga singlepiant of each as a stock culture, and thesewere grown at 16"C. 16 :8 h, 25 pmol photons'm-2 ' s-r with the light period digitally set to start at 0800 GMT. Plants were propagated vegetativelyby excising 2O(] M.D.GUIRY AND C.J.DAWES vegetativeapical portions of the plants, culture media and disheswere replacedevery 3-4 wk. ENRICHED SEAWATER
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