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The reproductive phenology ofnine species of Rhodophyta in thesubtidal region of the Isle of ManJoanna M. Kain (Jones) aa Department of Marine Biology, University of Liverpool, PortErin, Isle of ManVersion of record first published: 24 Feb 2007.

To cite this article: Joanna M. Kain (Jones) (1982): The reproductive phenology of ninespecies of Rhodophyta in the subtidal region of the Isle of Man, British Phycological Journal,17:3, 321-331

To link to this article: http://dx.doi.org/10.1080/00071618200650321

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Br. phycol. J. 17:321-331 1 September 1982

T H E R E P R O D U C T I V E P H E N O L O G Y OF N I N E S P E C I E S O F R H O D O P H Y T A I N T H E

S U B T I D A L R E G I O N OF T H E I S L E OF M A N

By JOANNA M. KAIN (JoNEs)

Department of Marine Biology (University of Liverpool), Port Erin, Isle of Man

Monthly samples of about 40 separate plants of each species were collected from 1 to 3 m below lowest astronomical tide on Port Erin breakwater, Isle of Man, Irish Sea. In three species growing on rock, Plocamium cartilagineum, Cryptopleura ramosa and Callophyllis laciniata, about 90~ of the plants were fertile in late summer but less than 10~ in spring although some fertile plants were always present. Delesseria sanguinea and Odonthalia dentata, also epilithic, had a winter sporing season, Odonthalia extending into late spring, and all plants were sterile in summer. Three species growing epiphytically, Palmaria palmata, Membranoptera alata and Phycodrys rubens, reproduced maximally in the first half of the year at the time when the stipes of the host species, Laminaria hyperborea, grow fastest. Only Palmaria had a sterile season, late summer. The encrusting Cruoria pellita showed little seasonality. The first three species, which reproduce mainly when the sea temperature is above average, are in the northern part of their geographical range. The remaining species (apart from Cruoria) reproduce mainly at low temperatures and are in the southern half of their ranges. Male plants appear to be in a minority in all species, presumably because they were manifest for a shorter period than carpos- poric plants. They appeared first after sterile periods and were absent as sporing declined. Plocamium and to a lesser extent Cryptopleura show an extremely high preponderance of tetrasporophytes in the population. This is attributed to perennation and some factor dis- allowing the survival of most of the tetraspores.

Within the subtidal forests of Laminaria hyperborea (Gunn . ) Fosl. of the northeast At lant ic live various species of red algae, some attached to the rock and some epiphytic on the stipes of the dominan t plant. M a n y of them are permanent members of the communi ty at any one site. How they are adapted to this env i ronment and why they are successful is o f considerable interest and studies of their biology will increase unders tand ing of the forest communi ty . As a first step the seasonality in reproduct ion in some of these species was investigated.

There are, of course, numerous records of fertility in subtidal red algae (e.g. Kjel lman, 1883; Brrgesen, 1902; Rosenvinge, 1924; Knigh t & Parke, 1931; Blackler, 1956). In most cases, however, they are non-quant i t a t ive and often spasmodic records. F r o m such it is not possible to tell whether there was adequate sampling in months for which no fertile plants are recorded. In order to achieve quant i ta t ive results here species c o m m o n all the year r ound were selected. This excluded seasonal annuals or erratic ephemerals.

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0006-1617/82/030321 + 11 $03.00/0 © 1982 British Phycological Society

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M E T H O D S

The nomenclature follows Parke & Dixon (1976). Plants were collected by hand from between 1 and 3 m below lowest astronomical tide on the

ruined Port Erin breakwater (54 ° 05.1'N, 4 ° 46-2'W). In order to sample mainly mature indi- viduals, plants in approximately the upper half of the size range were normally selected. If the size range was limited (in winter in some species) the largest available plants were taken. When a mixed phase population was sampled by selecting plants of mean size the results were not significantly different from those from the first method. Each plant or part of a plant was released into clear water and inspected to ensure that it was in only one piece before it was stored in a net bag. The next plant of the same species was collected from at least 1 m away. Samples of Cruoria were obtained by scraping a single fine ribbon off the rock with a diving knife tip and collecting this in a specimen tube.

Sampling was carried out every month, normally at least a week from the beginning or end, from October 1978 to September 1980. The aim was to collect 20 plants of each species on each occasion, to total 40 per month in the 2 years. However, as this was not always achieved and because some observations had to be rejected since male plants were not initially recognized, further collections were made in appropriate months up to March 1982. Observations during the different years were similar and the results have been pooled.

In the laboratory each plant (or part) was examined under a microscope for reproductive organs. As the aim of the work was to determine the seasonal change in the number of mature plants releasing spores into the environment the interest centred on tetrasporangia and car- posporangia. The species sampled are all dioecious so three types of plant would be expected: female gametophytes (only recorded when bearing the next phase, the carposporophyte), male gametophytes and tetrasporophytes. The exception to this was Palmaria where the female gametophytes are microscopic and transient with the tetrasporophyte arising directly.on the fertilized females (van der Meet & Todd, 1980). Active spore production in all species was judged from the appearance of the sporangia, i.e. when they were deep in colour, usually with dehisced examples. The plants were then recorded as fertile. No attempt was made to distin- guish males as functional; if they were detectable they were recorded. In the case of Cruoria a single c. 2 mm ~ portion of each ribbon of crust was squashed on a slide before microscope examination.

R E S U L T S

The n u m b e r of plants in each category, with apparent ly funct ional tetraspor- angia or carposporangia, or male plants were expressed as percentages of the total n u m b e r of plants of each species collected each month. These are shown as seasonal histograms in Fig. 1, with the total n u m b e r of plants observed shown over each column.

The first example in Fig. 1 is epilithic Plocamium cartilagineum. Fertile tetrasporophytes were present at all times of year bu t there was a marked sea- sonali ty with a peak in fertility in the a u t u m n and a distinct lack of fertile plants in the spring. Al though each mon th the a im was to collect mature, and therefore relatively large, plants, this could no t be achieved if they could no t be found. Thus while large Plocamium plants were a b u n d a n t in summer and a u t u m n they mostly disappeared dur ing the winter, so in spring only relatively small plants were examined. This might appear to be the reason for low fertility at that time. Evidence against this being the only explanat ion for the seasonality in this species will be presented in a later paper. The other obvious feature is the over- whelming preponderance of tetrasporophytes. Over 500 individuals from this site were examined before a gametophyte was found. In a further sampling p rogramme on Por t Erin breakwater and at Spanish Head (Kain, 1960) 4 km away, thalli of all sizes, no t necessarily spatially separated as in the month ly samples, were examined. The numbers are shown in Table I. A few gametophytes were found on the breakwater in December and Apri l bu t none in July, Septem-

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Reproductive phenology of subtidal Rhodophyta

Odonthoh~] [] M01e

[] Corposp.

[] Tetrasp. 4049 40

323

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Cryptopleura

:.:.

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Phycodrys

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Fz6. 1. The percentages of the plants of eight species which were fertile each month. The total number of plants observed each month is shown over the column.

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324 JOANNA M. KAIN (JONES)

ber or October. At Spanish Head, however, gametophytes were present in each quarter.

TABLE I. Total number of thalli of Plocamium examined and the numbers bearing tetrasporangia (T), carposporangia (C) and spermatangia (s) at various times at two sites at 1-3 m

Port Erin Breakwater Spanish Head Total T C S Total T C S

Sept./Oct. 1980 181 128 0 0 158 114 4 0 Dec. 1980 235 56 2 1 . . . . April 1981 430 74 4 7 299 90 8 4 July 1981 460 246 0 0 381 222 4 2 Oct. 1981 137 49 0 0 266 190 3 1 Dec. 1981 126 16 1 2 . . . .

A similar situation is seen in Cryptopleura ramosa (Fig. 1), another epilithic species. Again while the seasonal sequence could be partly explained by the growth pattern, later evidence has shown that even in April plants large enough to be fertile were present. Again tetrasporophytes predominated but gameto- phytes were found in most months.

In Callophyllis laciniata the maximum and minimum reproductive periods occurred about a month later than in the first two species (Fig. 1). Male plants were apparent only from June to November and not during the months of declining reproductivity. Gametophyte and tetrasporophyte phases were almost equally balanced.

In Delesseria sanguinea peak reproduction was later still, in mid-winter (Fig. 1). The fertile season was short, spores being produced only from December to March, though male organs appeared 3 months earlier. Again these were not apparent when reproductivity declined. There was no clear imbalance between the phases. This epilithic species and the next, Odonthalia dentata, are clearly and well known as perennials. There was no difficulty, therefore, in finding plants large enough to be mature at any time of year.

Peak reproduction in Odonthalia was later still, being in February/March (Fig. 1). The reproductive period was longer than in Delesseria, spores being available from November to June but with less than half the plants fertile in any month. Presumably there was more variation between individuals in the timing of their reproduction. Males were apparent for 3 months, half the carposporic period and preceding it by a month.

In Palmaria palmata most plants were reproductive during the first 5 months of the year, with about half the plants bearing tetraspores and most of the remainder bearing spermatia after January (Fig. 1). All were sterile from August to October. The plants sampled in this study were epiphytic, inhabiting the distal end of the Laminaria stipes.

The second species growing epiphytically, Membranoptera alata, was again mainly fertile in the first half of the year but there were no months of complete sterility (Fig. 1). Male plants were apparent in October and November, before carposporophytes appeared, and were absent in the reproductively declining months. The fact that tetrasporophytes constituted almost half the population from January to June and that almost a quarter of the plants were sterile, would

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Reproductive phenology of subtidal Rhodophyta 325

suggest that there was either an imbalance between the phases or the gameto- phytes were less fertile.

Phycodrys rubens, also growing epiphytically, was fertile all the year round with a minimum in October (Fig. 1). There seemed to be no pattern to the occurrence of male plants and these have since been found at the site in July and December. The apparent slight imbalance in the phases could have been due to size selection if tetrasporophytes are larger, a subject of further study.

The encrusting Cruoria pellita was sampled effectively for less than 2 years, the first 8 months of observations being discarded because males were not recog- nized. The results are therefore presented in a bimonthly histogram in Fig. 2. There seems little pattern to the reproduction except that males seem to be con-

J/F M/A M/J J/A $/O N/D

FIG. 2. The percentage of Cruoria scrapes fertile during 2-month periods from January/ February (J/F). Symbols as in Fig. 1.

fined to April to July. In the case of a crust it is impossible to define "a plant". In several cases a single squash contained both tetraspores and carpospores.

DISCUSSION

Seasonality in reproduction may be related to the geographical distribution of the species. Ptocarniurn cartilagineurn is widely distributed from Senegal to Nordland, Norway (Dixon & Irvine, 1977) in the north-east Atlantic, from Mexico (Abbott & Hollenberg, 1976) to Alaska (Lindstrom & Scagel, 1979) in the north-east Pacific and from Perth and Newcastle, Australia (Womersley, 1971) to at least Campbell Island (South, 1978) in the Southern hemisphere. Cryptopleura ramosa occurs only in the north-east Atlantic, from northern Mauritania (Gayral, 1966) to Shetland (Dixon, 1963), being absent from near Bergen in Norway (Jorde, 1966). Similarly Callophyllis laciniata extends from Morocco (Ardr6, 1970) to the Faeroes (BOrgesen, 1902), being absent from Iceland (J6nsson, 1912). Delesseria sanguinea occurs from Galicia, Spain (Niell, 1978) to north Norway (Jaasund, 1965). Odonthalia dentata has its southern limit offthe Isle of Man (Norton, 1978) and extends to Spitzbergen (Svendsen, 1959). In the west Atlantic it extends from Nova Scotia to Ellesmere Island (Taylor, 1957). Palmaria palmata is widely distributed in the northern hemisphere ex- tending from southern Portugal (Ardr6, 1970) to Spitzbergen (Svendsen, 1959) in the east Atlantic, from New Jersey to Ellesmere Island (Taylor, 1957) in the west, from southern California to Alaska (Abbott & Hollenberg, 1976)in the east Pacific and from the east coast of Korea (Kang, 1966), at least to Kam- chatka (Nagai, 1940) in the west. The southern limit in each case is between

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326 JOANNA M. KAIN (JONES)

35 ° and 40°N. Membranoptera alata occurs on both sides of the Atlantic, from Galicia (Niell, 1978) to north Norway (Jaasund, 1965) on the east and from north Massachusetts to Cumberland Sound (Taylor, 1957) in the west. Similarly Phycodrys rubens extends from north Portugal (Ardr6, 1970) to Spitzbergen (Svendsen, 1959) and from New Jersey to Ellesmere Island (Taylor, 1957). Finally, Cruoria pellita is confined to the east Atlantic between Tangier and Nordland, Norway (Dixon & Irvine, 1977). The approximate latitudinal ranges in the east Atlantic of eight of the species are shown in Fig. 3. Also shown are the month or months which are central to the main reproductive season of each species and the mean surface sea temperature off Port Erin, Isle of Man (from Slinn in Kain, 1971). It is clear that the three taxa with their centre of north/south range south of the Isle of Man (Plocamium, Cryptopleura and Callophyllis) reproduce mainly when the temperature is above the annual mean (10"7°C), while those with their centre of range to the north reproduce mainly when the temperature is below the mean. This phenomenon was observed some time ago in animals where, at 60°N, arctic-boreal species spawn in winter, boreal in

Isle of Man Temperature (*c)

Plocomium Oct, 13

Cryp/opleuro Sep./Oct. 13"5

Co/lophyllis Nov, 12

Delesserio don. 8.5

Odon/holio Feb./Mor. 7.5

Polrnorio Mor./Apr. 7'5

Membranoptera Mar. 7"5

Ph¥codrys Apr. 8

2~) 30 410 5=0 6=0 70 80 *N

FIG. 3. The approximate latitudinal ranges of eight species in the north-east Atlantic; the month(s) central to the main reproductive season on Port Erin breakwater and their mean surface sea temperature off the Isle of Man.

spring/summer and mediterranean-boreal in summer/autumn (Runnstr t~m, 1928). In both cases the temperature under consideration is that when reproduction occurs and not when it is initiated. While the former is important to the organism it must be linked in some way to the latter.

A corollary of the relationship between distribution and reproductive season may be a change in reproductive timing with latitude. Whether this occurs in algae is difficult to determine because of the lack of quantitative records. This is particularly so in cases such as Plocamium, Cryptopleura, Callophyllis, Mem- branoptera and Phycodrys, where, while there may be pronounced seasonality, reproductive organs can be found all the year round; non-quantitative records from other sites cannot be shown to differ. It is therefore necessary to take instead the species exhibiting sterile months in this site in the Isle of Man. There is no evidence that the compact season of reproduction in Delesseria differs with latitude although Bt~rgesen (1902) found early carposporangia in late October in

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Reproductive phenology of subtidal Rhodophyta 327

Iceland. However, unripe cystocarps were observed in November in the present work and Blackler (1956) recorded the organs for this month in St Andrews, Scotland. As Odonthalia is at its southern limit in the Isle of Man it might be a good example. In St Andrews (Blackler, 1956), Denmark (Rosenvinge, 1923) and Newfoundland (Hooper et al., 1980), the seasonality is similar but in Shetland (Dixon, 1963) and north Norway (Kjellman, 1883) both tetraspores and cystocarps were recorded in August. Kjellman stated that the species had not been found reproductive in winter in the Polar Sea. Here then is a possible example of a shift to summer sporing at higher latitude. Palmaria, on the other hand, produced tetraspores in Spitzbergen in winter and was sterile all summer in Nordland though there were many tetrasporangia in Novaya Zemlya in June and July (Kjellman, 1883) and they were recorded in Shetland in August (Dixon, 1963). This evidence is conflicting, perhaps because this species can occupy various habitats. This was the case in Japan where at one site the reproductive season was the same as in the Isle of Man but at another two it extended into August or September (Lee & Kurogi, 1972). The tetrasporic season in New Hampshire, U.S.A. was from October to July (Mathieson et al., 1981).

Quantitative data are available for Membranoptera alata and Phycodrys rubens on the other side of the Atlantic, off Maine at 43°N where, except near the surface in the summer, the water temperature is about 3°C lower than off the Isle of Man (Norall et al., 1981). Reproductivity is lower at most times of year. At four depths from 6 to 24 m Membranoptera had an almost completely sterile period from July to November, coinciding with reduced reproductivity in the Isle of Man. Phycodrys reproduced all the year at 6 and 12 m but only at 12 m did fertile plants number more than half the total at any time of year. At 24 m almost all the plants were always sterile. Both species were considerably shorter in length than those sampled in the Isle of Man. It might be suggested that these differences could be due to the species being closer to their southern limit than in the Isle of Man. Membranoptera, however, had an even shorter fertile period with May to November sterile at nearly 50°N in colder water in Newfoundland (Hooper et al., 1980). However, the species only occurred below 10 m depth at the site studied.

Norall et al. (1981) found significant differences in reproduction with depth in the four species they studied. They also considered plant stature to be important though the relationship with reproductivity was not consistent in their species. Both these attributes could clearly have an effect and current observations on most of the species considered at Port Erin include plant size measurements and in some cases depth ranges.

In the present study Plocamium, Cryptopleura, Callophyllis, Delesseria, Odonthalia and Cruoria were sampled from the rock while Palmaria, Mem- branoptera and Phycodrys were removed from Laminaria hyperborea stipes. It is unlikely that any of these species are obligate epiliths or epiphytes. Plocamium has often been recorded on other algae (e.g. Rosenvinge, 1931; Russell, 1968; Norton et al., 1969) and was described as a characteristic epiphyte in Iceland by B~Srgesen (1902). Cryptopleura is a common component of the L. hyperborea stipe flora on the Carrick Rock off Port St Mary, Isle of Man, 9 km (by sea) from Port Erin breakwater (Harkin, 198I). Similarly Callophyllis has been re- corded on stipes in other parts of the British Isles (Norton et al., 1969; Norton,

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328 JOANNA M. KAIN (JONES)

I972). In eastern Scotland both Delesseria and Odonthalia were recorded on stipes (Norton, 1976) while B/Srgesen (1902) mentioned the former as a common epiphyte on L. hyperborea stipes in Iceland. Even the encrusting Cruoria has been found on stipes (Norton, 1970, 1972). Of those treated as epiphytes in the present work, Palmaria is a well known epilith in the lower intertidal, Mem- branoptera occurs on rock (e.g. Irvine et al., 1972) and Phycodrys is common on rock on Port Erin breakwater though at a much lower abundance than on the stipes. It is possible that these last three species are able to make use of the stipes as a substratum because their peak sporing seasons span the period when stipes grow fast in length (Kain, 1976), producing new available stipe surface area. The most advantageous time for inhabitants of shallow subtidal rock to produce spores would appear to be winter when there is most available vacant rock surface. In fact all the species considered here were reproducing in midwinter, though this was not necessarily their peak period.

There are numerous records of the predominance of the tetrasporophyte phase in red algae. Dixon (1965) pointed out that in Europe tetrasporic plants are often reported from further north than sexual plants. The absence of the sexual phase may be due to a non-Polysiphonia-type life history as in some mem- bers of the Corallinaceae (Chihara, 1975), or it may indicate vegetative propaga- tion as in Callithamnion corymbosum (Whittick, 1978) and Antithamnion cruciatum (Whittick & Hooper, 1977). Recent quantitative phenological work has demonstrated a less severe imbalance between the phases: sexual plants form a small proportion of the population. Examples of this are in four species of Hypnea (Mshigeni, 1976; Rama Rao, 1977), two species of Polysiphonia (Kap- raun, 1978), two species of Gelidium (Montalva & Santelices, 1981) and one species of Gracilaria (Hoyle, 1978). Provided that the existence of a Polysiphonia- type life history is not doubted there are two possible explanations for an obser- ved imbalance. Firstly, the sexual plants could be shorter lived than the tetra- sporophytes. This could be an annual phenomenon as in Dumontia incrassata (Kilar & Mathieson, 1978) or the tetrasporophytes could perennate while the sexual plants were ephemeral. The second explanation is that more carpospores per parent survive to maturity than do tetraspores per sporophyte. A steady state with the phases in any proportions can be postulated using appropriate survival ratios (Fig. 4). The fact that it is usually tetrasporophytes which pre- dominate is presumably associated with the diploid state being the robust one, genetically better able to respond to stress, local or geographical. An example of the effect of local stress is on Ptilota serrata Kuetz. off Maine where the propor- tion of tetrasporic plants increased with depth (Norall et al., 1981). It is possible

@ . > cr' @" > 9 ¢.1N ("~ • ~ C Carposporophytes

d .o,. 0=.,o0..,.

FIG. 4. Diagrammatic representation of a steady state situation in a population of tetrasporophytes (®), female gametophytes (~) supporting carposporophytes (C) and male gametophytes (~) of equal longevity but where 2 spores per 4 tetrasporophytes sur- vive and 4 carpospores borne on each female gametophyte survive.

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Reproductive phenology of subtidal Rhodophyta 329

that the predominance of Plocamium tetrasporophytes in the present study is associated with the species being in the centre of the northern half of its distribu- tion. It is also influenced by a local effect, however; some factor on the outside of Port Erin breakwater is more stressful than at Spanish Head. It seems likely that the means whereby tetrasporophytes predominate so effectively is a mixture of the two possibilities postulated above. Firstly the plants clearly perennate: regeneration from procumbent and upright thalli is obvious. "Colonies" of two species of Plocamium, consisting of patches of interconnecting basal stolons bearing individual fronds were similarly observed at 15 m off southern Australia (Shepherd, 1981). Secondly, tetraspores, copiously produced, must usually fail to survive on apparently suitable rock surfaces. The same probably applies to Cryptopleura.

Tveter-GaUagher et al. (1980) noted that male plants appear in lower numbers than female plants because of difficulty in recognizing them (in the early stages) and partly because the organs by which they can be distinguished are shorter lived. Recognition was initially found to be a problem in some species in the present work but once male plants had been identified positively they were easy to distinguish, sometimes with the naked eye. A shorter life for male organs is to be expected, it is only necessary for them to span the period of presence of car- pogonia. In the present work the recorded fertile period of the female plants was that of carpospore release, probably prolonged, following the development of the carposporophyte. The presence of male organs would thus be expected to precede the appearance of cystocarps, possibly with a gap between the periods. While males appeared first after a sterile period, a gap, if it existed, was masked either by the failure to recognize antheridia as spent or by individual variation in time with consequent overlapping. The consistently lower proportions of male plants is evidence for their shorter fertile period (if proper recognition is assumed).

Recording the presence of ripe and apparently dehiscing sporangia does not give an indication of the rate of release of spores or of the number released per plant. The latter clearly varies greatly: some plants are almost covered with stichidia or tetrasporangial sori, others bear only a few. The timing can only be estimated when populations are reasonably synchronous as in Delesseria. Other species may be fertile over long periods either because tetrasporangia (or car- posporangia) production continues or because release is slow. Another aspect not investigated was whether apparently functional sporangia were actually liberating spores. The presence of vacant tetrasporangial sites can be taken as good evidence and in most cases apparently ripe cystocarps liberated spores when squeezed gently. Most of these species have been used in culture work and spores obtained from them when they appeared to be fertile. Finally, no attempt was made to quantify spores rather than plants bearing them.

ACKNOWLEDGEMENT

Michael Bates, an exceptionally reliable diver, assisted with almost all the collections, fre- quently under distinctly uncongenial conditions.

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DIXON, P. S., 1965. Perennation, vegetative propagation and algal life histories, with special reference to Asparagopsis and other Rhodophyta. Bot. gothoburg., 3: 67-74.

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(Accepted 15 March 1982)

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