Phycologia(1984) Volume 23 (3),357-367

Photoperiodicand temperatureresponses in the reproductionof north-easternAtlantic Gigartinu acicularis (Rhodophyta:)

M.D. Gunv aNo E.M. CuNNrNcneu

Department of Botany, University College, Galway, Ireland

M.D. Gurnv eNo E.M. CuNNrNcn,qu(1984) Photoperiodic and temperature responsesin the re- production ofnorth-eastern Atlantic Gigartina acicularis (Rhodophyta: Gigartinales).Phycologia 23:357-367.

Gigartina acicularis (Roth) [.amour., a predominantly intertidal red alga,has only rarely been found with reproductive structuresin the British Isles and northern France.Elsewhere in the north-eastern Atlantic, reports of cystocarpic plants are largely from November to February while those of tet- rasporangialplants are from July to October. Male and female plants formed gametangiaonly at daylengthsof 12 h or lessand at temperaturesof 14-18"C.Photon exposures>1.5 mmol m 2 of incandescentlight, given in the middle of a 16 h dark period at l6.C, completely inhibited cystocarp formation, although some carpogonial brancheswere formed at up to 3.34 mmol m 2. Five pho- toperiodic cycles of 8:16 h at 16oCwere the minimum necessaryto induce the formation of car- pogonial branchesand cystocarps.Carpospores gave rise to plants which formed tetrasporangiaat daylengthsof 16,12, l0 and 8 h at 16'C. The precisephotoperiodic and temperaturerequirements for gametangialreproduction in G. acicularis result in gameteformation being limited to autumn in north-easternAtlantic populations.It is suggestedthat, in the northern part ofits range,populations of G. acicularis are largely maintained by vegetative propagation. As one goes further south the gametangialreproductive 'window' gradually enlargesdue to higher ambient temperaturesin the autumn. The paucity ofrecords oftetrasporangial plants in the British Isles,however, needsfurther investigation. This is the first report ofphotoperiodic control ofgametogenesisin the Rhodophyta and the responsewould appear to be true and absolute.

INTRODUCTION lantic will not hybridize. These difficulties of identification have been compounded by the vir- Gigartina acicularis (F.ot}r) Lamouroux [see Dix- tual absence of reports of reproductive material on and Irvine (1977) for changein nomenclaturel of G. aciculans, particularly in the north-eastern (Rhodophyta) is a narrow, terete to slightly flat- Atlantic. In the British Isles cystocarpic plants tened, sparingly branched species found in in- have apparently been found only once (Devon tertidal or shallow subtidal habitats in the At- in January 1829; material in BM) and records of lantic and the Mediterranean. It grows most tetrasporangial plants are also very rare (Galway commonly on rocks in sheltered, silty situations, Bay, November 1966; material in GALW). Else- where it often forms conspicuous turfs. In the where in the eastern Atlantic reproductive rec- Atlantic the species has been reported from the ords for G. acicularis are as follows: Gayral ( I 966) British Isles south to Cameroun and from North reported cystocarpic plants from November to Carolina south to Uruguay (Dixon & Irvine 1977). February on the north coast ofFrance; Seoane- Some difficulties have been experienced in dis- Camba (1965) found cystocarpic plants in Jan- tinguishing between certain forms of this species uary and February on the north coast of Spain, and G. teedii (P.ott') Lamouroux, a species with and tetrasporangial plants in July, August and a similar geographical distribution in the north- September; in Portugal, Ardr6 (1969) collected eastern Atlantic. Forms intermediate in mor- tetrasporangial plants in October but did not re- phology have frequently been reported (Harvey port any other reproduction; Gayral (1958) re- 1833;Gayral 1958; Hoek & Donze 1966; Dixon ported cystocarpic plants from August to March & Irvine 1977),but Guiry (1984) has shown that on the coast of Morocco. In the British Isles, cultured plants of these two species from the At- casual examination of populations by one of us

357 358 Phycologia, Vol. 23 (3), 1984

(M.D.G.) over the past decade has revealed not modiflcation in Mclachlan (1973) except that a single fertile plant. Cystocarpic and tetraspo- the disodium glycerophosphate concentration was rangial plants were, however, common at Sines reducedby halfl. Due to a bacterial contaminant, and Sagres, Portugal in January 1977, and cys- a spore-forming Bacillus specieswhich now seems tocarpic plants were abundant at La Toja, Gal- to be common in many laboratories culturing icia, Spain in January 1978. The available phe- marine algae, and which is resistant to a wide nological data on the formation of cystocarps in range of antibiotics (West & Guiry unpubl. data), G. acicularis suggested a photoperiodic response plants were later grown in a modification of Von similar to that described by Liining ( I 9 80, I 9 8 I a, Stosch's medium (VS). Our VS is composed of 198lb) for the formation of tetrasporangia in the equal volumes of the following stock solutions Trailliella-phase of Bonnemaisonia hamifera (all in 500 ml glass-distilled water): 21.26 g Hariot. Llsing cultured plants isolated from the NaNOr; 2.68 g Na, or-beta-glycerophosphate; north coast of France and from the south coast 0.139 g FeSO.'7HrO; 0.98 g Mn Clr'4HrO; 1.86 of England we here attempt to explain the re- g Naz EDTA'2H'O;0.05 g Biotin; and 0. I g productive periodicity of G. acicularls and the Aneurine HCI and 0.2 mg Vitamin B,r. Two me- lack of records of reproductive plants from the dia types are made up from this stock solution: British Isles. A preliminary account of this study haltstrength VS, to which l0 ml of VS solution was given in Guiry and Cunningham (19E3). is added to each litre of sterilized seawater and quarter-strength, to which 5 ml is added. The absence of a TRIS buffer in VS may help to re- MATERIALS AND METHODS duce bacterial contamination (cf. van der Meer I 982). Initial attempts to isolate Gigartina acicularis Photon flux densities were measured using a into culture using plants collected in January in LI-COR Model 185-8 meter and a LI-I90SB Portugal (1977) and Spain (1978) were unsuc- quantum sensor. Light sources were directly cessful owing to necrosis (cf. West & Guiry 1982, above the cultures and reflected light from the p. 206), which is enhanced by the use of full- sides and bases ofthe culture cabinets was taken strength, enriched seawater media. Tetrasporan- into account in all measurements. Fluorescent gial plants of Gigartina acicularis were collected light was provided by cool-white 65180 W tubes; in the lower intertidal at Santec, a few kilometres incandescent light was provided by 60 W house- west ofRoscoff, on the north coast ofFrance on hold tungsten bulbs. Temperature was measured l5 September 198 1. Cultures (isolate 382) were using nickel-chromium/nickel-aluminium ther- established from tetraspores released overnight mocouples immersed in 250 ml distilled water. at room temperature (approx. 15'C) and inocu- (This was the volume ofthe culture medium used lated onto glass slides using a fine Pasteur pipette. in the temperature experiments.) In all studies The plants were initially grown in a north-facing temperature is expressed as the variation found window at the Station Biologique de Roscoffwith in these volumes of water. frequent changes of unenriched sterile seawater. A preliminary study of a field population of The resulting sporelings were transported to Ire- Gigartina acicularis atNew Quay, Co. Clare, Ire- land in a cooled container. Additionally, plants land (53"09.5'N, 9o05'W) was carried out from were isolated vegetatively from G. acicularis September 1982 through April 1983. The site populations from mid-intertidal pools at I(im- was visited at fortnightly intervals. Plants were meridge Ledges, Dorset, UK in April 198 1 (iso- sampled haphazardly within a 0.025 m'z fixed late 371). Whole plants were transported to Ire- quadrat. These samples were examined micro- land in sterilized seawater in a cooled container. scopically in the laboratory for reproduction. Growing tips were excised and cultured in en- Seawater temperatures were taken at the turn of riched seawater at low photon flux densities (3- the tide. 2 5 rrmol m s-t) at 16 + 1'C, 16:8 h until the Seawater temperatures for the period 1974- plants were free of algal contaminants. 1981 were obtained from the Shellfish Research Plants were grown in several types ofenriched- Laboratory, Carna, Co. Galway, which is about seawater media throughout this study but for 75 km due west of the New Quay site. Temper- each experiment the medium type was standard. ature is continuously recorded at the intake point Initially, plants were grown in quarter-strength for the Laboratory's seawater pumps. Daylength Provasoli's Enriched Seawater [PES; West's readings were obtained for Shannon Airport, Co. Guiry and Cunningham: Gigartina acicularis 359

Clare which is about 70 km south of the study continuously. Male and female plants were iso- site. lated into separate culture for further investiga- tion of the photoperiodic response.

Effects of temperature on cystocarp RESULTS formation Growth of plants in culture Stock cultures of male plants of isolate 382 from Franceweremaintainedat l6 + 1'C, 8: l6 h, 20 Vegetativeplants from Britain (isolate371) grown pmol m-2 s-r, and female plants were grown at in full-strength media becamegreen distally and 16 + 1"C, 16:8 h, 20 pmol m-2 s-t, for at least ultimately died. Eventually, it was found that one month beforehand. Under these conditions quarter-strengthPES or VS would support the males formed an abundance of spermatia and A single vegetative plant was isolated $owth. the females did not form carpogonial branches. which when 25-30 mm long grew at 5-7 mm per Each experimental culture dish contained one weekat 16 + 1'C, t6:8 h, 20-25p.molm-2 s-1. pretreated male and flve pretreated female plants. Plantsgrown from this isolate did not reproduce The dishes were then placed at 8:16 h, 20-30 over a period of 8 months under these condi- pmol m-2 s 1,at each of the temperatures shown tions. On transferring some of these plants to in Table 1. Plants were examined at regular in- l6 + l"C, 8:16 h, 20 pmol m-2 s-t, spermatan- tervals with a dissecting microscope; cystocarps gia were formed after 8 days whereasplants re- were deemed to have formed when a noticeable tained at 16:8 h remained sterile. Growth was bulge was apparent on the thallus surface. After slowerunder this short-dayregime, only 1-3 mm I 7 days all cultures were transferred to I 3 + l'C, of new tissue being formed each week on plants 16:8 h, 20 pmol m-' s-t, to await the devel- 25-30 mm long. These plants resembledthe opment of cystocarps, at which time the male French isolate describedbelow but had a lighter plant was also removed. Cystocarps (Figs 3a, b) colour (Figs 4a--c). were formed only in cultures maintained at 14- Tetraspores released from field plants from l8oC inclusive (Table l), and were formed most France(isolate 382) had formed small discsabout rapidly, 7-9 days after the start of the cross, at 100 pm in diameter on arrival in our laboratory. 16"C. Carpospores were not released in most in- After 15days at 16 + l'C, t 6: 8 h, 25 pmolm-2 stances although carposporophytes were present s-rin quarter-strengthPES, discs about 150pm in all cystocarps sectioned. A transfer to l0oC is in diameter had single upright fronds up to 200 generally necessary for carpospore release. A rep- pm long and both discs and uprights had a few licate experiment at loC intervals from 16 to hyaline hairs up to 250 pm long. Upright fronds 20oC gave similar results. Controls maintained grew rapidly, reaching 4 mm long (discs to 400 at l6 : 8 h at l6 and l0'C did not form cystocarps. pm) after 29 days. At 57 days the plants were about I 7 mm long but no reproduction had taken Effects of daylength and night-breaks on place.Some plants were then transferredto l6 + formation of gametangia 1"C,8:16 h,20 prmolm-2 s-r. After 13 days under this regime spermatangiaand carpogonial Plants (isolate 382) were preconditioned as de- brancheswere apparent on separateplants but scribed in the previous section. One male and plantsretained at 16 + loC, 16:8 h, 25 pmol five female plants were placed in each dish and m-2 s-r remained sterile. Carpogonial branches were then grown at 16 + l'C, 20-30 pmol m-'z were formed on new tissue at the apices of the s-t, at the photoperiods shown in Table 2. The main axes and the lateral branches; the fertile cultures were monitored at regular intervals and area was often distinctly swollen (Figs la, b). were removed to non-inducing conditions (16 + Trichogynes were easily observed as very large l"C, 16:8 h, 20 trrmolm-2 s-t) after 17 days. numbers were formed and they protruded 150- Cystocarps were formed only on female plants 350 pm beyond the surfaceofthe thallus. Sper- subjected to daylengths of 12 h and less (Table matia could be clearly seenadhering to the tri- 2). Cystocarps were formed most rapidly, and in chogynes,even under a dissecting microscope. larger numbers, at daylengths of 8 h. There would Spermatangiawere formed in a continuous sonrs seem to be a gradual increase in the time nec- 4-5 mm below the apices(Figs 2a, b) which, after essary for formation and a reduction in the num- the cuticle had been shed, released spermatia ber of fertile plants with increasing daylength 360 Phycologia,Yol. 23 (3), 1984

Table 1. Effectsof temperatureon cystocarpformationin Gigartina acicularis(strain 382 from France).Numbers indicate number of planis forming cystocarpsin a dish of five plants. All cultureswere given an 8 : 16h photoperiod at21-30 pmol m-2 s-t for 17 daysat the temperaturesshown and werethen transferredto 16 + 1'C, 16:8 h, 25 rrmolm-2 s-r

Tempera- No. ofdays from start ofcross ture (+1'C) lt TJ t5 t7 25 32 39 40 24 ZJ 22 20 19 18 1 245 16 1A 5 l6* I 45 5 t4 1 5 555 l3 I2 l0 10r * Repeat.

(Table 2). Night-breaks in the middle of a 16 h spores, despite having being maintained at 15 night blocked reproduction, even when they con- and I 0'C for I 4 weeks after the conclusion ofthe sisted of only 10 min of incandescent light at 20 experiment, and eventually degenerated without pmol m-2 s 1.However, in one of three replicate releasing spores. Trichogynes were not apparent experiments carried out at different times using on any ofthe plants g.rown at daylengths of > 12 h, a I h night-break with fluorescent light at 30 however, increasingly larger numbers were pmol m-2 s-t a single cystocarp was formed after formed at daylengths of =12 h. It, unfortunately, 39 days (Table 2); this cystocarp did not release proved impossible to quantify this effect. How-

Table 2. Effects of photoperiod on cystocarp formation in Gigartina acicularis (strain 382 from France). All cultures were grown at 16 + 1'C. Numbers indicate number of plants per dish of five plants forming cystocarps after the specifiedperiod

Photo- period (h) No. ofdays from start ofcross (ight: Night dark) break u l3 t5 t7 25 JZ 16:8 16:8* 14:10 ; 12:12 ;; ; t;; t2..12* 1l 1111 I 10:14 I JA 4555 5 l0:14 J+ 5555 5 8: 16 2 45 5555 5 8:16* I4 5555 5 8:16 t h 8:16 t h*t 1 I 8:16 I h*t 8 : 16 30 min* 8:16 10min{ t Repeat. 2 f Fluorescentlight at 30 pmol m s ' used as the night break. 2 I f Incandescentlight at 20 pmol m s used as the night break. Guiry and Cunningham: Gigartina acicularis 361

10mm

3 l-r 4 F-,1 10mm 10mm

Figs 1-4. Morphology of fertile plants of Gigartina acicularis from France and England in culture. Figs lq b. Female plants of isolate 382 from France. The plants were grown for severalmonths at 16 + 1'C, 16:8 h and then transferred to 16 + 1'C, 8:T6- h; carpogonialbranches are forming in large numbers in the swollen areaspresent at most of the tips. These branchesmore or less ceaseelongation and swollen tissue is formed continuously. Somebranches resume growth and becomeacicular (arrow); thesehave smaller numbers of carpogonialbranches. Figs 2aob. Male plants of isolate 382 from France. Spermatangialsori are forming at the tips (arrow). These plants were grown continuously under 16 + 1'C, 8:16 h; plants grown under long-day regimes are generally broader. Figs 3a, b. Female plant of isolate 382 from France forming cystocarpsat 16 + 1'C, 8: l6 h. The female plants were grown under a photoregime of 8:T6- h prior to the introduction of a male plant, note the differencein morphology between theseplants and those shown in Figs la, b, which were initially g.rownat 16: I h. Figs 4a-c. Male plants of isolate 371 from England grown continuously at 16 + l'C, 8:T5 h; spermatangial sori are forming at the tips. 362 Phycologia,Vol.23 (3), 1984

Table 3. Number of cyclesof 8 :T5 h photoperiod necessaryto induce cystocarpformation in Gigartina acicularis (isolate382 from Frante). Plants were transferredfrom an 8:T6 h photoregimeat 16 + l'C after periods varying iom I to 9 days (e indicates time of transfer).Numbers of plants (of five) forming cystocarpsare indicated

Number of days from start of cross

7 8 9 11 13 15 t7 18 25 )L 39 46

e- e- e- o-25555 e-135555 e-135555 o-12355555 e123555555

ever, the number of cystocarps formed is clearly being transferred to 16:8 h and fragmented eas- a reflection ofthe number oftrichogynes. ily, so that the numbers of plants with cystocarps In order to determine the number of photo- could not be assessed.Cystocarps were apparent periodic cycles necessary for the formation of in all dishes after 14 days; they were formed in cystocarps, male plants (isolate 382) were pre- small numbers (l-3 per dish), and there was no conditioned as described in the previous section pattern to their frequency ofoccurrence. for at least two months prior to the start of the It seems likely from these results that despite experiment. One fertile male plant and five ster- the preconditioning of the male plants at l6:8 h ile female plants were placed in each of nine for two months prior to the start of the experi- 2 culture dishes at l 6 + l'C, 8 : T6-tr, 20 trrmolm ment, spermatangia were forming from sper- s-r. One dish was removed to 13 + loC, 16: matangial mother cells induced prior to this. I h, at 24 h intervals for nine successive days. Spermatangia In Gigartina species are diftcult quan- Cultures were examined at regular intervals over to detect, especially when present in small plants a period of 46 days. All plants formed cystocarps tities. Although none were seen when the except those kept at 8:15 h for l-4 days (Table were examined at the beginning of the experi- 3). It is clear from Table 3 that the greater the ment, we are inclined towards the opinion that number of photo-inductive cycles, the more rap- some were forming as there was no pattern in idly the cystocarps are formed. Again, inhibition the frequency ofoccurrence ofcystocarps as was of carpogonial branch formation seemed to be found in the reciprocal experiment (Table 3). responsible for the effect. the number ofcycles In an attempt to determine Night-break photon exposure effects necessary for the formation of spermatangia, male plants (isolate 382) were preconditioned for two Two male plants forming spermatangia and flve (isolate months under non-inducing conditions at 16 + preconditioned sterile female plants 382) l'C, 16:8 h, 20 pmol m-2 s r. Female plants were placed under a 8: 16 h photoregime with a were also preconditioned for two months under t h light break in the middle of the 16 h dark period provided the same temperature and irradiance levels as period. The main 8 h lieht was p.rr^ol the males but at 8:16- h. At the end of this time, by cool-white fluorescent light at 16-25 given in- the female plants were forming numerous car- m-2 s-t but the light break was by an pogonial branches in swollen areas at the tips of candescent bulb at photon flux densities of0.09- I the branches. The experiment consisted of three 20 pmol m-2 s (Table 4). male plants and three female plants placed in Cystocarps were formed only at the lowest each of six dishesat l6 + l"C, 8 : T6 h, 20 pmol photon exposures of 0.64 and 0.32 mmol m-2; m-2 s 1,with one dish removed to non-inducing at the former exposure only one plant formed conditions every 24ll for 6 days. The male plants cystocarps and only two were produced on this were removed after 14 days, at which time no plant; at the latter four plants eventually formed spermatangia were apparent. The female plants cystocarps but only a few were produced on each exhibited a high degree ofnecrosis shortly after plant. The control, which did not receive any Guiry and Cunningham: Gigartina acicularis 363

Table 4. Night break photon exposuresnecessary for the inhibition of carpogonialbranch and cystocarpformation in Gigartina acicularis (strain 382 from France).Two male plants forming spermatiaand five sterile femaleplants were placed at 16 + 1'C, with a I h light break in the middle of a 16 h night. The light break was provided by a tungstenbulb aI the irradiancesshown. The males were removed after 17 days and the female plants transfered to 13 t l.C, 16:8h,25pmolm 2s-r.Numbersindicatethenumberofplantsformingcystocarps;t:trichogynes observed

Photon flux Photon No. ofdays from start ofcross density exposures (pmol m '?s-t) (mmol m-2) IJ 15 t9 ZJ zo 30 42 20 72 10 36 5 18 2 7.2 0.93 3.34 ;; 0.42 1.5l t tt 0.l8 0.64 t t I 1l 0.09 0.32 t t J 44 Control 0 3 5 5 5 55

night-break, formed numerous cystocarps rap- all conditions tested, including a night-break re- idly on all plants. Trichogynes were formed in gime. Shorter daylengths did tend to result in small numbers on plants receiving photon ex- more rapid reproduction but the differences in posures of 3.34 and l.5l mmol m-2 (Table 4) timing for these mature plants were slight (Table but no cystocarps were formed on these plants; 5). Plants forming tetrasporangia were trans- presumably the incidence of occurrence was too ferred to 10 + l'C at 16:8 h and 8: 16 h. The low to allow fertilization to take place. At photon short-day regime caused almost immediate ces- exposures of 7.2 mmol m 2 and above, neither sation of tetrasporogenesis but under the long- trichogynes nor cystocarps were formed. Unfor- day regime the plants continued to form and tunately, it is impossible to count trichogyne release numerous tetraspores for about 6 weeks numbers because they are clustered too closely and then ceased. together and the terete nature ofthe plant makes microscopic examination diflfrcult. Preliminary field studies

At the New Quay study site, a large population Effects of daylength and temperature of G. acicularus occurs on silty rocks, boulders on tetrasporogenesis and stones at mean low water neap tides down Female plants of Gigartina acicularis from France to extreme low water spring tides in the area of (isolate 382) crossed to male plants from England a rapids system. No reproduction of G. acicularis (isolate 371) formed cystocarps which released was observed during October 1982 through April carpospores at 10 but not at 15 or 20oC. These 1983. Temperature and daylength measure- spores gave rise to plants similar in morphology to the gametangial plants except that they were darker in colour and less frequently branched. + Initially plants were grown at 16 l'C. t 6: I h. Table 5. Number of days to tetrasporerelease in ma- 20-25 pmol m-2 s-r. On reaching ll mm long ture tetrasporangialplants of Glgartina acicularis, grown at74 days, three plants were transferred to l6 + under diferent photoregimesat 16 + l'C l'C, 8:16 h, 2O-25 p,molm-'s-t, tetrasporangia Number of days were formed on plants 14.5 mm long after 15 Photoregime days. Plantsretainedat l6: I h did not, however. (h) ll form tetrasporangia for a further 49 days and 16:8 13 only one plant formed tetrasporangia on this oc- l2:T2 JJJ casion. Sterile plants from this culture were l0:1-4 I JJJ transferred to a variety of photoregimes at 16 + 8:T6- I 333 a:/-):l:/.) JJJ I"C (Table 5). Tetrasporangia were formed under 364 Phycologia,Vol. 23 (3), 1984

I x

t0^ o d

Fig.5. Temperature and daylength curves for Galway Bay in 1982. Data from temperaturereadings taken at the ShellfishResearch Laboratory, Carna,Co. Galway and from the field study site at New Quay (Sept.-bec.).Vertical unbroken lines indicate inhibition ofgametangial reproduction in Gigartina acicularis by daylengthsof >12 h; horizontal broken lines indicate inhibition bv temoerature < 14.C.

ments show (Fig. 5) that in the autumn of 1982 of cystocarps. Some short-day flowering plants water temperatures fell too rapidly for the for- require only a single inductive cycle, however, mation of gametangia. most require a minimum of 12 inductive cycles (Vince-Prue 1975). Photoperiodic algae re- ported to date, all ofwhich have been short- day plants, require 5-12 inductive cycles (Dring DISCUSSION & West 1983). (2) A low-energy night-break in the middle of Gigartina acicularis is yet another marine alga a long night inhibits the response. Because of which shows a clear photoperiodic response. It problems with handling large numbers of G. is the first red alga reported to show a combi- ecicularis plants it is difficult to pinpoint the nation of photoperiodic and temperature control 500/oinhibition point accurately; it is, however, of gamete formation; all previously reported in- clear from Table 4 that a night-break photon stances have been in the formation either of exposure of 1.15 mmol m-2 of tungsten white meiosporangia or of erect fronds. In the few in- light causes inhibition of cystocarp formation. stances where short-day induction of gameto- (3) Once the initial response has been induced, genesis has been reported it has not been estab- removal to non-inducing conditions does not lished whether these are true photoperiodic inhibit further development. This is princi- responses. The only other marine red alga with pally shown by the experiments in which plants an isomorphic life history for which a true pho- forming cystocarps continue to develop under toperiodic response has been shown is Haly- long-day conditions. Furthermore, sperma- menia latifoliaKitzing (Maggs & Guiry 1982). tangial formation continues in sori induced The response in G. acicularui is clearly a true under short-days although no new sori are photoperiodic one, and is similar to that found formed. Similarly, carpogonial branches are in many flowering plants. This is confirmed prin- only formed on tissue produced under short- cipally by three features: day conditions; no new carpogonial branches (l) Five cycles ofinducing conditions are suf- are formed when a transfer to long-days is ef- ficient for a clear-cut response in the formation fected. Guiry and Cunningham: Gigartina acicularis 365

Table 6. Seawatertemperatures at the intake point ofthe ShellfishResearch Laboratory, Carna, Ireland for the period 1974-81. Readingsrepresent means ofternperatures taken in the last two weeksofSeptember and the first two weeksof Octoberl standard deviations of the meansare also given (SD)

September October SD Max. Min. SD Max. Min. t974 r 3.0 0.8 14.8 t2.l I 1.5 0.5 r2.5 I 1.0 1975 r 3.9 0.6 14.6 t2.'7 13.2 0.7 13.8 I 1.6 1976 t3.7 0.6 14.4 t2.6 t2.8 0.8 t4.4 I 1.5 r977 t2.8 0.8 14.1 rt.7 r0.5 0.4 rt.4 t0.2 1978 14.8 1.3 16.5 12.5 t3.4 0.5 r4.5 r 3.0 1979 r3.8 0.7 15.0 t2.4 t4.l 0.4 14.8 13.5 I 980 t4.9 0.5 ts.7 14.0 t2.0 1.6 t4.7 10.5 198I 14.1 0.5 15.1 I J.J I 1.6 1.3 14.5 t0.4

Although we have shown that five cycles of 8: vations at New Quay indicated that no repro- 16 h photoperiod at 16 + l'C is the minimum duction took place in a large field population. number of cycles necessary for the formation of The available phenological data on the repro- mature, receptive carpogonial branches, we have duction of this species in the British Isles since not been able to work out the number of cycles it was first found in 18l I suggest that reproduc- necessary for the formation of spermatangia. It tion has been extremely rare. One must, how- seems likely that spermatangial sorus formation ever, bear in mind that G. acicularis is a rela- is under photoperiodic control but sori induced tively uncommon plant which is confined to south under short-day conditions continue to form and south-western coasts, and that field phyco- spermatangia when transferred to long-day con- logical activity tends to be at its lowest ebb in ditions. December to February. Gametogenesis in G. acicularis is conflned to The virtual absence ofreports oftetrasporan- a relatively narrow temperature and photoperiod gial plants from the British Isles is more difiicult range (14-18'C inclusive; night lengths >12 h) to explain because the formation of tetraspo- which has interesting seasonal effects. This com- rangia does not seem to be limited by daylength. bination of conditions confines the formation of No tetrasporangial plants were found at the New gametangia to the autumn. As one goes further Quay study site during the period September 1982 north in the Atlantic this reproductive 'window' to April 1983. Tetrasporangial plants do occur becomes progressively smaller, eventually reach- in this population as plants isolated vegetatively ing a point where reproduction in a population into culture formed tetrasporangia; these tetra- may take place only when higher-than-average sporangia released viable tetraspores that devel- autumn temperatures allow induction. This as- oped into male and female plants which have sumes, of course, that latitudinal ecotypes do not more or less the same photoperiodic response as exist, a possibility that should not be discounted that described in this paper for plants from Brit- as such ecotypes are now known in two tany (Guiry unpubl. data). Further studies are fDumontia contorta (S.G. Gmelin) Ruprecht; needed to elucidate the conditions (particularly Rietema & Breeman 1982 and Halymenia lati- temperature) necessary for the formation of tet- folia Kitzing; Maggs & Guiry unpubl. datal. rasporangia in field and cultured plants. Analysis of autumn temperature data taken near Liining (1980, 1981a, 198lb) has shown a pho- the known northern limit of Gigartina acicularis toperiodic/temperature response in the forma- in the Atlantic (Roundstone, Co. Galway) for the tion of tetrasporangia in the Trailliella-phase of period 1974-81 (Table 6) suggests that sexual Bonnemaisonia hamifera which is very similar reproduction was theoretically possible only in to the control of gametogenesis in G. acicularis. the autumns of 1978, 1979 atd, perhaps, 1980; In B. hamifera tetrasporogenesis is confined to in all other years for which data are available, daylengths of 11 h and less and to temperatures temperatures dropped below l4'C before day- of 15-17'C inclusive. [No tetrasporangia were lengths of 12 h were achieved (late September; formed at 10, 12,20 or 23"C (LiiLning l98lb).] Fig. 5). In I 982, seatemperatures dropped below At Helgoland, in the North Sea, gametophytes 14'C before the end of September, thus blocking of B. hamifera are only found sporadically in the any gametangial reproduction. Our field obser- wild (Kornmann & Sahling 1977); in 1968 and 366 Phycologia,Vol.23 (3),1984

1969 they were common and Li.inine (1980) logique de Roscoffand Dr J. Cabioch for facilities points out that in 1966 and 1967, September provided in September l98l; to the National water temperatures at Helgoland were higher by Board for Science and Technology, the Royal 0.7-O.8'C than the l0 year mean for this month. Irish Academy and the Centre National de la Re- Liining (1980), citing Feldmann (1957), stated cherche Scientifique, France for a travel grant to that only tetrasporophytes of B. hamifera have visit Roscoff; to M.J. Dring and C.A. Maggs for been found on Scandinavian coasts. Rueness helpful discussion; to D. Brown for providing (1977), however, records the occurrence of ga- temperature data; to P. Cooke for help with pho- metophytes in Norway; presumably these occur tography; and particularly to Wendy Guiry, sporadically on Scandinavian coasts in the same without whose assistance maintenance of these way that they do at Helgoland. In this regard it cultures would be impossible. This paper rep- is interesting to note that although the shell-bor- resents contribution no.244 from the School of ing phases of Helminthocladia calvadosii (La- Marine Sciences, University College, Galway. mouroux) Setchell and Scinaia forcellata Bi' vona-Bernardi were found recently by Kormann and Sahling (1980), the gametophytes have not REFERENCES been collected there since the beginning of the present century. Apnn6 F. 1969. Contribution d l'6tude des alguesma- Dixon (1965, 1973) has pointed out that a rines du Portugal I. La flore. Port. Acta biol., s€r. B l0: 137-555. number of algae near the northern limits of their CuLr-rNeNrJ.P., Eoaw B. & Wnsr-e.NP. 1980.Most distribution in the British Isles are unknown in northern fruiting record of Pterosiphoniacomplan- a reproductive state, notably Pterocladia capil- ata (Clem.) Falkenb. on the Atlantic coast. Ir. Nat. lacea (5.G. Gmelin) Bornet et Thuret and Bor- J. 20: 140-141. 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