Studies on the Biosystematics and Ecology of the Epilithic Crustose Corallinaceae of the British Isles

British Phycological Journal

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Studies on the biosystematics and ecology of the Epilithic Crustose Corallinaceae of the British Isles

Walter H. Adey & Patricia J. Adey

To cite this article: Walter H. Adey & Patricia J. Adey (1973) Studies on the biosystematics and ecology of the Epilithic Crustose Corallinaceae of the British Isles, British Phycological Journal, 8:4, 343-407, DOI: 10.1080/00071617300650381

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Download by: [UNAM Ciudad Universitaria] Date: 23 June 2016, At: 12:15 Br. phycol. J. 8:343-407 31 December 1973

STUDIES ON THE BIOSYSTEMATICS AND ECOLOGY OF THE EPILITHIC CRUSTOSE CORALLINACEAE OF THE BRITISH ISLES

By WALTER H. ADEY and PATRICIA J. ADEY National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A. CONTENTS Page Introduction 343 Methods and Materials 344 List of Stations 345 Systematic List 346 Keys I. Generic Key 348 II. Vegetative Key to Species 348 IlL Reproductive Key to Species 350 IV. Anatomical Key to Species 352 Biology Lithothamnium 353 Mesophyllum 361 Phymatolithon 365 Leptophytum 376 Lithophyllum 380 Tenarea 392 Fosliella 397 Ecology 400 Acknowledgements 405 References 406 INTRODUCTION The present study is part of a biosystematic-ecological investigation of the crustose corallines of the North Atlantic begun in 1960; it will be incorporated in abbreviated form into an extensive monographic treatment covering the entire North Atlantic region, planned for publication later in the present decade. In this paper, we present new data for the British Isles and discuss the relationship of the British coralline flora to that of the northern North Atlantic as a whole. Epilithic species occurring from the British Isles northward, in the eastern North Atlantic, are treated from a biosystematic point of view. Ecologically, the

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 British flora is examined in detail with reference to previous publications by the first author on Norway (Adey, 1971), Iceland (Adey, 1968) and the western North Atlantic (Adey, 1966c). In the course of this investigation, material was also collected from French and Spanish coasts. These collections have been compared to the British flora, and tentative conclusions are discussed. However, until the Mediterranean and W. African coasts can be examined in detail to provide an equivalent frame of reference, the French and Spanish work cannot be considered complete. The focal point of this paper is the epilithic coralline flora. Bottom coverages of maerl or rhodolith (see Adey & Macintyre, 1973) apparently require a somewhat different quantitative approach from that used in rocky areas. For example, our unpublished studies in Vigo Bay (see, however, Adey & McKibbin, 343 344 W. H. ADEY AND P. J. ADEY

1970) indicate that the ecological variation involved is greater than on rocky bottoms and, for consistent results, sampling density probably must be considerably greater. Although in subarctic and boreal waters the species composi- tion of rhodoliths is relatively simple, with two Lithothamnium species in the north (L. glaciale Kjellman, subarctic; L. tophiforme Unger, arctic) and Phy- matolithon calcareum (Pallas) Adey et McKibbin and Lithothamnium corallioides Crouan frat. dominant in the south, it appears that a number of temperate elements enter the maeri flora on the west coast of Ireland. In this area we collected at a single maerl locale (Galway Bay) and have also seen several small collections from Kilkiernan and Clew Bays. Phymatolithon calcareum and Lithothamnium coraUioides (and, locally in the north, Lithothamnium glaciale) are likely main elements in the British maerl. However, in the southwest perhaps as many as three additional species are involved. The situation is apparently complex, and we do not feel that we can cover adequately the maerl flora of the southwestern British Isles without further study of the Irish, French and Spanish maerls, and perhaps also those of the Mediterranean. We have, however, briefly discussed the maerl flora, and included P. calcareurn and L. corallioides in the keys. For additional taxonomic-ecological information and references to the literature on P. calcareum and L. corallioides, see Adey & McKibbin (1970) and Cabioch (1966). The British Isles Corallinaceae have not previously been the subject of intensive study by a coralline specialist. Foslie collected at Roundstone, Ireland (Foslie, 1899) and the Isle of Wight (Foslie, 1892), and received from his British con- temporaries some specimens for identification (Foslie, 1895, 1906). Madame Lemoine also received collections from Clew Bay, Ireland (Lemoine, 1913) and Rockall (Lemoine, 1923) and of course has studied the French flora extensively (see for example Hamel & Lemoine, 1952). The various lists compiled by British workers, e.g. Holmes & Batters (1890); Batters & Murray (1891); Batters (1892, 1896, 1902); Newton (1931); Anon. (1952); Parke & Dixon (1968); are primarily based on Foslie's and to some extent Lemoine's identifications. Where this was not the case, considerable doubt can be attached to the validity of the identifications. The works of Foslie and Lemoine form the primary phytogeographic- historical base for this study. No attempt has yet been made to sort out the validity or meaning of identifications in the subsidiary literature.

METHODS AND MATERIALS

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 The locations of transect stations (maerl stations in parentheses) occupied during the course of the study are shown in Fig. 1 and a list is given below. Most were worked in standard depth zones (0-3 m, 3-9 m, 9-15 m, 15-21 m, 21-28 m, 28-37 m, 37-46 m) using SCUBA and the techniques employed in the earlier regional studies (see Adey, 1966c, 1971). In the text that follows, depths of less than 5 m are called shallow, depths greater than 20 m deep. Collections from the stations in Scotland and those off Belfast, Cork and Falmouth were obtained during the summers of 1967 and 1968 using our vessel "Bjorneng". The Galway Bay stations were occupied in December of 1968 using a local chartered boat. Those on the Isle of Man, off southwestern Wales, Plymouth and Portsmouth were occupied during November-December 1970, using the facilities of several marine stations. The collections made in November and December were necessary to obtain reproductive material of Phymatolithon, the dominant genus of the British flora. The collections of crustose corallines kept at the British Museum were studied in London, during December 1970, together with material from the Robertson Herbarium on loan from Glasgow Museum. Those requiring preparation were obtained on loan. In the results presented below, the identifications and collection localities are incorporated along with the quantitative Biosystematics and ecology of epilithic crustose Corallinaceae 345

• ¢7-17

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I FIG. 1. Transect stations in the British Isles (see List of Stations below for key).

data obtained from the present field studies. Museum information is included on the charts (X) only where it extends a species limit. This has affected the quantitative data appreciably in only one case, that of Mesophyllum lichenoides (L.) Lemoine where the plant is primarily epiphytic in the British Isles and increasingly epilithic to the south. All of the other species discussed here are only very rarely epiphytic. The biosystematic studies and ecological identifications are primarily based on the micro-

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 tome sectioning of selected specimens fixed live and preserved at the time of collection. Some sectioning of dried material was also done later where identification problems existed. Susa's fixative, standard paraffin wax sectioning procedures, and phosphotungstic haematoxylin staining were used in all cases. It should be noted that the British Isles data are given as station percentages (in the zones indicated) in the distributional maps presented below, and the western North Atlantic data and Icelandic data are given as regional means (after Adey, 1964, 1965, 1966a, 1966b, 1966% 1968). Norwegian data are treated by station and are taken from Adey (1971).

LIST OF STATIONS Shetlands: east side of Luna Ness, 60°25'N, l°5'W Sta. No. 67-17, 18 August 1967 Orkneys: east side of Westray, 59°17'N, 2°52'W Sta. No. 67-18, 25 August 1967 67-19, 26 August 1967 346 W. H. ADEY AND P. J. ADEY

Northwest Scotland: Summer Isles, southwest corner Tanera More, 58°0"4'N, 5°25"2'W Sta. No. 67-20, 29 August 1967 Loch Broom (dredged), 57°55.6-59.8'1,4, 15.5-26'W Sta. No. 67-21, 1 September 1967 Hebrides, north of Loch Eport, 1'4. Uist, 57°34'N, 7°7'W Sta. No. 67-22, 4 September 1967 Loch Linnhe, northwest Lismore Is., 56°32-7'N, 5°28-8"W Sta. No. 67-23, 7 September 1967 Irish Sea: Belfast Lough, northwest of Mew Is., 54°42'N, 5°31"W Sta. No. 67-25, 11 September 1967 Isle of Man, south and east 54°3-11'1',1,4°25-47'W Sta. Nos. 70°8, 9, 10, 6-12 December 1970 Ireland: South Coast, southwest of Cork, 52°43.8'1,4, 8°19'W Sta. No. 67-26, 15 September 1967 West Ireland, Galway Bay, 53°11-14'N, 9°0-17'W Sta. Nos. 68-36, 11-13 December 1968 (68-37 inner Galway Bay) Wales: Pembrokeshire, mainland inside Skomer, 51°44.2'N, 5°14.6'W Sta. No. 70-11, 18 December 1970 England, South Coast: East side Lizard Head, 50°0.8'N, 5°5.3'W Sta. No. 67-27, 22 September 1967 Falmouth Harbour (dredged), 50°8-10'1,4, 5°2-4'W Sta. No. 67-28, 23 September 1967 Plymouth, 56°19'N, 4°8-15"W Sta. Nos. 7002, 4, 26-27 November 1970 The Solent, Hayling Is.; north side Isle of Wight; Swanage, 50°38-46'N, 0°59'-1°55'W Sta. Nos. 7005, 6, 7, 30 November-1 December 1970 East Scotland, off Aberdeen, 57°6.1'N, 2°4"2'W Sta. No. 68-26, 21 August 1968

SYSTEMATIC LIST The suprageneric classification used below is that of Adey & Johansen (1972). Probable synonymies are indicated, and questionable or possibly rare species not found in this investigation or in the herbarium collections are discussed. Detailed descriptions of each species are given below.

Subfamily Melobesioideae (Areschoug) Mason

Tribe Melobesieae Areschoug Lithothamnium Philippi emend. Adey 1966b Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 L. glaciale Kjellman (incl. L. colliculosum Foslie; L. granii Foslie) L. sonderi Hauck L. corallioides Crouan frat. Mesophyllum Lemoine 1928 M. lichenoides (Linnaeus) Lemoine Clathromorphum Foslie emend. Adey 1965 C. (Lithothamnium) compactum (Kjellman) Foslie was reported by Lemoine (1913) for Clew Bay. This plant is, however, an arctic species, not found in our European field studies even in Norwegian waters. The similar C. circumscriptum (Stromfelt) Foslie does occur in north and east Iceland (Adey, 1968) and in northern Norway (Adey, 1971). Biosystematics and ecology of epilithic crustose Corallinaceae 347

However, in Norway it occurs only in the fjords, its southern limit (in trace amounts) being Trondheimsfjord. Johnson & Hensman (1899) reported a Foslie-determined specimen of C. circumscriptum from Iceland. However, there is no British material of any Clathromorphum in the Foslie Herbarium (Adey & Lebednik, 1967). The nearest reported specimen in the Foslie Herbarium is a single plant from the Faeroes, and as that was not sectioned, it too remains questionable (see also Bargesen, 1902). Recent laboratory and field studies have indicated that C. circumscriptum requires winter temperatures below 2-3°C to reproduce (Adey, 1973). Thus, its occurrence in the British Isles seems quite doubtful, except possibly as a late Pleistocene relict population in very restricted inshore waters. It was not found in our collecting nor seen in the herbarium collections. Without microtome sections or considerable field experience with both species, young plants of Litho- phyllum orbiculatum can be confused with Clathromorphum circumscriptum. We suggest that this is the explanation for its earlier citation in the British literature.

Tribe Phymatolitheae Adey et Johansen Phymatolithon Foslie emend. Adey 1964 P. polymorphum (Linnaeus) Foslie P. laevigatum (Foslie) Foslie P. rugulosum Adey P. lenormandii (Areschoug) Adey P. calcareum (Pallas) Adey et McKibbin Leptophytum Adey 1966b L. laeve (Stromfelt) Adey (Lithothamnium bornetti Foslie is a Phymatolithon or Leptophytum species, vegetatively quite similar to and possibly a variety of Phymato- lithon polymorphum. The mature asexual conceptacles are raised. It occurs, apparently in small quantities, in the southern British Isles and on the French and Spanish coasts. However, we have been unable to obtain enough reproductive material to adequately describe and classify the plant and, in the quantitative ecological data, it is included with that for P. polymorphum. We regard this case as the major unsolved

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 problem within the epilithic coralline flora.)

Subfamily Lithophylloideae Setchell Lithophyllum Philippi 1837 L. incrustans Philippi L. orbiculatum (Foslie) Foslie L. nitorum sp. nov. Tenarea Bory 1833 T. hapalidioides (Crouan frat.) comb. nov. T. confinis (Crouan frat.) comb. nov. 348 W. H. ADEY AND P. J. ADEY

Subfamily Mastophoroideae (Svedelius) Setchell Fosliella Howe 1920 F. valida sp. nov. F. tenuis sp. nov.

KEYS I. GENERIC KEY 1. Tetrasporangia and bisporangia with thick-walled caps; asexual conceptacles multipored 2. Meristem cells elongate, perithallial cell elongation occurring mainly in the meristem, conceptacle cap only epithallial; conceptacle primordium developing in vegetative meristem 3. Lithothamnium-type epithallium, meristem cells with caps, hypothallium non-coaxial Lithothamnium 3. Non-Lithothamnium-type epithallium, meristem cells without caps, hypothallium usually coaxial Mesophyllum 2. Meristem cells short, perithallial cell elongation progressive, conceptacle cap perithallial--conceptacle primordium vegetative in perithallium 4. Conceptacle caps thin (1-3 cells), pore cells present in asexual conceptacles, gonimoblasts developed marginally in conceptacles Leptophytum 4. Conceptacle caps thick (> 4 cells), pore cells absent in asexual conceptacles, gonimoblasts scattered over conceptacle centre Phymatolithon 1. Tetrasporangia and bisporangia without caps, all conceptacles single-pored 5. Secondary pits present in perithallium 6. Hypothallium a single layer of curved, elongate cells Tenarea 6. HypothaUium multilayered or a single layer of short cells Lithophyllum 5. Cell fusions present in perithallium Fosliella

II. VEGETATIVE KEY TO SPECIES (for use with x 30- x 50 dissecting microscope) This key is intended to provide identification for perhaps 75 ~ of sublittoral epilithic crustose coralline coverage. Small plants, < 1-2 cm ~, can be especially difficult until one has considerable experience, and a key to cover all possibilities would be too complex. For instance the "branching" species sometimes do not have branches when small or near their depth limit, and their occurrence as smooth crusts is not included here. It is very difficult to describe adequately the Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 difference between an irregular crust growing over substrate irregularities and a normally branched plant with young branches, especially since Lithothamnium glaciale often initiates its branches over substrate projections. Unless reproductive structures are present or anatomical characteristics are obvious on vertical fracture, small plants, those found in deep water (other than the usually obvious Lithothamnium sonderi) and otherwise "peculiar" plants should be microtome sectioned before attempting identification. Anatomical characteristics used in the vegetative key are those that can be seen with a x 30- x 50 dissecting microscope on a vertical fracture, preferably made perpendicular to the growing margin. Best results are usually obtained by removing a chip near the plant margin with a sharp instrument. The fracture should be fresh and as nearly Biosystematics and ecology of epilithic crustose Corallinaceae 349

vertical as possible. Colour descriptions refer to material that is alive or has been quickly dried in the shade. 1. Plants distinctly branched (branches > 2-3 mm long) (if plants are from > 5-10 m depth and branches are small, watch for the evanescent conceptacles of Lithothamnium sonderi) 2. Plants pink-violet and usually unattached Phymatolithon calcareum 2. Plants pink, free or attached 3. Branches less than 1.5 mm in diameter, numerous, plants somewhat irregular and usually small Lithotharnnium eorallioides 3. Branches greater than 1 mm in diameter, plants generally becoming large and often with smooth regular branches Lithotharnniumglaeiale (Note: P. ealcareum, especially small plants and those from deep water receiving relatively little light, may not develop the usual pink-violet colouration. In a typical maerl collection from shallow water, 5-10 ~ of the plants may have to be sectioned for identification. In deeper water (10-20 m) perhaps 20-30 ~ would have to be sectioned.) 1. Plants not distinctly branched, or branches very small (L. sonderi) or very irregular and broad (P. polymorphum) 4. Crusts imbricate, and sometimes leafy (margins not adherent) 5. Hypothallium coaxial (see Newton, 1931, Fig. 190d) as seen on radial vertical fracture Mesophyllum liehenoides (Although M. liehenoides is commonly epilithic in France and Spain, in the British Isles it is mostly epiphytic on Corallina or growing over a coarse substrate of dead Corallina and other debris.) 5. Hypothallium not coaxial 6. Perithallial cells large, layered; easily visible from surface or on fracture Tenarea confinis 6. Perithallial cells small and no anatomical structure obvious with the dissecting microscope Phymatolithon lenormandii 4. Crusts fully adherent, not overgrowing 7. Surface appearing hard and/or glossy 8. Faint white rings or discs (conceptacle remains) scattered on surface Lithothamnium sonderi 8. White rings absent 9. Surface rugulose Phymatolithon rugulosum 9. Surface rugose to smooth 10. Crust thick, well developed, "flowing" appearance, pink-violet* Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Phymatolithon polymorphum 10. Crust relatively thin, pink-orange 11. Surface without ridges Lithophyllum nitorum 11. Surface with ridges 12. Ridges near margins, concentric, not white; conceptacle cavities or traces > 300 ~m in diameter Leptophytum laeve

* If not dried rapidly and kept dry, most crustose corallines will gradually alter their colour to a light green or yellow. Phymatolithonpolymorphum alters easily to a light green colour and this will appear frequently in collections where other specimens still maintain a somewhat faded but more normal colour. This feature can be diagnostic. 350 W. H. ADEY AND P. J. ADEY

12. Ridges scattered over surface, randomly orientated, often white-capped; conceptacle cavities or traces <; 300 ~m in diameter Phymatolithon laevigatum 7. Surface appearing chalky and/or granular 13. Crusts thick (> 200 ~m) and extensive at maturity 14. Plants yellowish, or if pink, appearance chalky; conceptacles generally present and sunken 15. Perithallium usually distinctly layered; conceptacles in section as Fig. 2A. Lithophyllum orbiculatum 15. Perithallium not distinctly layered, conceptacles (except male) in section as Fig. 2B. Lithophyllum incrustans 14. Plants pink or purple and surface appearing granular; conceptacles often present and raised 16. Violet or brown coloured Tenarea confinis 16. Bright red-orange coloured Tenarea hapalidioides (Note: Lithophyllum tortuosum (Esper) occurs on the French coast and perhaps is to be found in southwestern England, especially in the Scilly Isles, and in southwestern Ireland. It is a chalky, yellow-violet crust, occurring near the low water mark, and has margins tending to turn up with meeting of adjacent crusts and often developing a plate-labyrinth structure. Its conceptacles are small and sunken, the cells are small with no obvious layering in either hypothallium or perithallium.) 13. Crusts thin (< 200 ~m) and only 1-2 cm in diameter at maturity 18. Crusts transparent or nearly so, 1-3 cells thick Fosliellatenuis 18. Crusts not transparent, up to 10-15 cells thick Fosliellavalida

A B C D E FIG. 2. Shapes of conceptacles in vertical section. A. Lithophyllum orbiculatum, B. Litho- phyllum incrustans, C. Phymatolithon rugulosum, D. Phymatolithon polymorphum, E. Phymatolithon [aevigatum. Ill. REPRODUCTIW KEY TO SPECIES (conceptacles present--all diameters refer to cavities) Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 1. Conceptacles primordial (pore or pore plates not visible) and with a distinct white cap (Phymatolithon) 2. Branched and generally unattached Phymatolithon ealcareum 2. Crustose 3. Caps breaking out as distinct white lens-shaped bodies Phymatolithon polyrnorphum Phymatolithon laevigatum (see other keys) 3. Caps thin or fragmenting 4. Conceptacles and caps sunken Phymatolithon rugulosum 4. Conceptacles and caps raised Phymatolithon lenormandii Biosystematics and ecology of epilithic crustose CoraUinaceae 351

1. Conceptacles mature (pore or pore plates visible) or if primordial, with thin and indistinct caps. 5. Conceptacles multipored (Note: In Phymatolithon considerable care and 30-50 x magnification may be needed to distinguish a multipored roof from the surface) 6. Conceptacle roofs raised above surrounding surface 7. Conceptacles > 700 ~m in diameter Mesophyllumliehenoides 7. Conceptacles 700 ~m or less in diameter 8. Conceptacles 400-700 ~.m in diameter Leptophytum laeve 8. Conceptacles < 400 ~zm in diameter 9. Conceptacles generally white, evanescent, leaving faint rings when breaking out Lithothamnium sonderi (Note: A possible form of P. polymorphum ("Lithothamnium" bornetii) hasraised conceptacles and these become white as they degenerate. However, if these are broken off, the cavity can be seen to project into the crust. The conceptacle cavities do not project into the crust in L. sonderi.) 9. Conceptacles generally colour of living plant, long lasting, leaving distinct craters if breaking out at all Lithothamniumglaciale Lithothamnium corallioides Phymatolithon lenormandii (see other keys) 6. Conceptacle roofs level with or below surrounding surface 10. Plants branching and usually free Phymato#thon calcareum 10. Plants crustose 11. Conceptacles without a raised rim (usually a sunken rim, Fig. 2C) Phymatolithon rugulosum 11. Conceptacles with a raised rim as in Fig. 2D PhymatoOthon polymorphum or Fig. 2E Phymatolithon laevigatum (also see other keys) 5. Conceptacles single-pored 12. Conceptacles with a distinct rim 13. Margins very thin, virtually transparent Fosliella valida 13. Margins thick (Phymatolithon spp., see 10 & 11) 12. Conceptacles without a rim 14. Conceptacles sunken, plants chalky 15. All conceptacles as Fig. 2A, small; perithallium layered, hypo- Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 thallium single layer Lithophyllum orbiculatum 15. Asexual and cystocarpic conceptacles as Fig. 2B, perithallium not layered, hypothallium sometimes coaxial Lithophyllum incrustans (see vegetative key No. 18, note on Lithophyllum tortuosum) 14. Conceptacles raised 16. Plant surface "hard", not granular--cells not distinctly visible at x 50 17. Surface highly glossy Lithophyllum nitorum 17. Surface dull (return to 7, this key) 16. Plant surface granular--cells visible at x 50 18. Crusts thin and often transparent Fosliella tenuis 352 W. H. ADEY AND P. J. ADEY

18. Crusts not transparent, even at margins 19. Colour violet or brown Tenarea confinis 19. Colour orange Tenarea hapalidioides

IV. ANATOMICAL KEY TO SPECIES The anatomical key to species can be used on microtome sections with any stain, but best results are obtained with phosphotungstic haematoxylin; living and liquid preserved material give best results--the critical epithallial and meristematic structures are often lost in dried material. 1. Secondary pits in perithallium 2. Perithallial cells elongate, 2-10 diameters long Tenarea sp. (see vegetative key) 2. Perithallial cells isodiametric, less than 2 diameters long 3. Hypothallium coaxial Lithophyllum incrustans 3. Hypothallium single-layered 4. Perithallial cell-layering marked Lithophyllum orbiculatum 4. Perithallial cell-layering weak 5. Epithallium one cell thick, meristem short Lithophyllum nitorum 5. Epithallium several cells thick, meristem elongate Lithophyllum incrustans 1. Secondary pits absent (cell fusions present) 6. Hypothallium a single cell layer, crusts thin Fosliella spp. (see vegetative and reproductive keys) 6. Hypothallium multilayered, crusts or branches well developed 7. Hypothallium coaxial Mesophyllum lichenoides 7. Hypothallium irregular 8. Meristem cells elongate, Lithothamnium-type cover cells 9. Staining bodies present Lithothamniurn sonderi 9. Staining bodies absent Lithothamnium glaciale Lithothamnium corallioides (see vegetative key) 8. Meristem cells short, Phymatolithon-Leptophytum-type cover cells 10. Staining bodies present 11. Branching Phymatolithon calcareum I I. Crustose 12. Hypothallium generally > 40 ~zm thickness Phymatolithon polymorphum Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 12. Hypothallium generally < 30 ~m Phymatolithon laevigatum (If intermediate, see vegetative and reproductive keys) I0. Staining bodies absent 13. Perithallial cells large, rounded, > 7 ~zm diam. Leptophytum laeve 13. Perithallial cells smaller, more angular, < 7 ~tm in diameter Phymatolithon lenormandii Phymatolithon rugulosum (Phymatolithon polymorphum) (see vegetative and reproductive keys) Biosystematics and ecology of epilithic crustose Corallinaceae 353

BIOLOGY Lithothamnium Philippi 1837 Species of Lithothamnium are the dominant elements over a broad range of mid-depths in arctic waters. It has frequently been reported that they are also important in tropical seas. However, recent ecological studies have indicated that this is generally true only in deep water (Adey & Macintyre, 1973). Since the transfer of all of the former Antarctic species of the genus to Mesophyllum or Leptophytum (Adey, 1970a), the Antarctic area appears to be devoid of species of Lithothamnium. Approximately two thirds of the Lithothamnium species represented in the Foslie Herbarium show well developed branches, and only 14~o are known exclusively as smooth or mammillate crusts. Two of the three British Isles species, Lithothamnium glaciale and L. corallioides, are strongly branched. The third, L. sonderi, usually shows some vague signs of branch development and occasionally is found with abundant, though short and simple, branches.

Distribution Lithothamnium sonderi is the primary deep water coralline in the British Isles (Figs 3, 4A). It was found at all of our stations which extend deeper than 15 m, except in the Shetlands, and frequently reached abundances of over 70~, relative to the total coralline flora of the zone, in the deepest zones. At the Isle of Man, Belfast and Loch Broom it comprised more than 97 ~ of the crustose corallines in the 28-37 m zone. It was not found in Iceland and occurred only in Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

NoR,H A, LAN,,C OCEAN

...... _ .... 7

FIa. 3. Geographical distribution of Lithothamnium sonderi in the northern North Atlantic. Stations S. Mean relative abundance in y., 15-37 m. Note: at the Aberdeen, Scotland station, the deepest zone collected from was 15-21 m. L. sonderi composed 33 ~ of the coraltines in that zone. It is probably considerably more abundant at greater depths, so the data for this station have been omitted. British Isles abundance is indicated by station. W. Atlantic abundance is indicated by region. 354 W, H. ADEY AND P. 3. ADEY

very small amounts in the southern part of North Norway. However, in southernmost Norway and to a lesser extent the Bay of Biscay, it is of considerable importance in deep water. It has been reported from the Mediterranean (Hamel & Lemoine, 1952), but relatively infrequently, suggesting a continuing reduction in abundance to the south and east. L. sonderi is not known from the western Atlantic. Since it is quite distinctive and generally easy to identify, it probably does not occur, even in trace quantities. It has been suggested (Adey, 1971) that the distribution of L. sonderi in the northern North Atlantic is limited by low winter temperature levels. An inability to withstand mid-winter temperatures below 6-7°C could explain the limiting of its northern distribution pattern. Lithothamnium glaciale is probably the most abundant coralline in mid- to deeper water in the North Atlantic subarctic (Figs 4B, 5). It extends from Cape Cod and the British Isles northwards and develops strongly on bedrock or boulder bottoms. It also grows well on pebble and shell bottoms, where wave or

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.Q I I 1 I o 12 I I I I ~ ~0 "6 B

I0 I I 1 0 I 20 30 40 50 Depth (m) FIG. 4. Depth distributions of epilithic Lithothamnium species in the British Isles, mean all stations. A. Lithothamnium sonderi. B. Lithothamnium glaciale.

current motion is consistent but not excessive. Larger fragments broken free of the rock substrate and exposed to medium wave energy or the tidal currents in Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 fjords and bays (see Adey & Macintyre, 1973) sometimes develop nodules (rhodoliths) which can form extensive deposits. L. gla¢iale is the primary subarctic rhodolith builder, being partly replaced by Lithothamnium tophiforme in arctic waters and by Lithothamnium eorallioides and Phymatolithon ealcareum in British waters. In Britain L. glaciale occurred in our collections mostly in Scotland and especially in the western sea lochs (to 36 % in Loch Linnhe), but also, in smaller quantities, in stations at exposed areas (Fig. 5). The most southerly record in our collections is the Isle of Man; small specimens, however, were also seen in the Irvine collection from Lundy (Irvine, Smith, Tittley, Fletcher & Farnham, 1972). On the east coast, L. glaciale has been found at least south to Berwick. It has Biosystematics and ecology of epilithic crustose CoraUinaceae 355

...... '"NORTH ATLANTIC OCEAN...... ~"J@ ~~0~ ......

FIG. 5. Geographical distribution of Lithothamnium glaciale in the northern North Atlantic. Mean relative abundance in %, 15-28 m. Recorded as in Fig. 3.

been reported from the French side of the English Channel (Hamel & Lemoine, 1952; as L. granii), but apparently based only on identifications of earlier workers and so some question remains.

Descriptions of species Lithothamnium sonderi Hauck: Thin, reddish plants usually flat-surfaced with occasional low and narrow (1-3 mm) mounds, sometimes developing simple branches, 1-3 mm in diameter and several mm long; generally attached to small pebbles and shells, though occurring on ledge and boulder substrates in deep water, never found living unattached; hypothallium subparallel to substrate, 15-50 ~m thick, cells 10-15 Fm long, 3.5-9 ~zm in diameter; perithallium developed from a frequently elongate meristem cell layer, the cells of which are 2-5-7 ~m long, 3.5-6 ~m in diameter; eighth perithallial cell is 3.5-7.7 Fm long, 4-6-5 ~tm in diameter; epithallium box-shaped with typical Lithothamnium-type "ears" in section, cells 1.5-2.5 ~m long, 2-5-5 Fm in diameter; pit bodies distinct, Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 0.25-1.5 ~m in diameter, staining bodies usually numerous, up to 2.5 ~zm in diameter; mature asexual tetrasporic conceptacles raised 45-115 ~m above the surrounding thallus, cavity 160-315 ~m in diameter; male conceptacles raised 90-160 ~zm, cavity 160-295 ~tm in diameter; female conceptacles raised 115-190 ~zm, cavity 145-170 Fm in diameter; mature cystocarp not seen; alI conceptacle roofs evanescent but with a persistent marginal ring. (Data: British, French and Spanish specimens.)

Lithothamnium glaciale Kjellman: Crusts initially thin but often becoming extensive and thick, usually with abundant regular or more often irregular branches; colour reddish, generally with numerous small white speckles; 356 W. H. ADEY AND P. J. ADEY

especially abundant on small pebbles and shells, but occurring on all hard substrates and often continuing growth when detached, forming beds of rhodoliths (maerl); hypothallium subparallel to substrate, 15-50 ~tm thick, cells 7.5- 26 ~m long, 3-8 ~zm in diameter; perithallium developed from an elongate meristem cell layer, the cells of which are 3-8 ~m long, 4--8 ~m in diameter; eighth perithallial cell 8.5-12 ~zm long, 4-8 ~m in diameter; epithallium "Lithothamnium type" 1.5-3 ~zm long, 3.5-7-5 tzm in diameter; pit bodies very small, up to 0.5 ~m in diameter, mostly spherical, but sometimes plate- or ring- shaped; no staining bodies; tetrasporic or bisporic asexual conceptacles usually slightly raised, up to 100 ~m high, cavities 150-360 ~tm in diameter, sporangia with thick apical walls (multipored); male conceptacles raised 145-220 ~m, cavities 295-430 ~m in diameter; female conceptacles raised 180-225 tzm, cavities 295-325 ~m in diameter; cystocarpic conceptacles raised 135-320 ~m, cavities 385-520 ~m in diameter; all conceptacles eventually buried by perithallial growth or more often breaking out. (Anatomical data: British Isles and southern Norway; reproductive data: Iceland, Norway and British Isles.)

Lithothamnium corallioides Crouan frat. : To date we have found this plant living unattached only (see section on ecology below). It is described in detail by Adey & McKibbin (1970). Neither of the two rock-encrusting species of Lithothamnium present in the British Isles poses persistent identification problems. L. sonderi is generally easily recognised by its ephemeral white conceptacles or, after breakout, by the residual ring or very slight tissue depression. This species also exhibits a distinctive, glossy, undulating texture which becomes apparent to the consistent observer. This is a useful indicator in the relatively few cases where traces of conceptacles are completely lacking. L. glaciale is the only well developed, attached, branching, crustose coralline in the region. Even where it is quite thin, its white speckled, finely irregular red surface is usually distinctive. In section, the epithallium and meristem serve to identify the genus and the absence of staining bodies quickly distinguishes L. glaciale from L. sonderi. Although hypothallial cell diameters are about the same in the two species, cell lengths are greater in L. glaciale and in general the hypothallium is better developed (Table I). The highly glossy and

TABLEI. Hypothallial cell measurements (~tm), Lithothamnium Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Diameter Length Thicknessof layer Measurementsfrom: (number) max. mean rnin. max. mean min. max. mean rain. cells plants stations L. glaciale 11.5 6.5 3 26 14.3 7.5 65 31 15 99 33 23 L. sonderi 9 6.4 3.5 15-5 11.6 8.5 50 25 15 21 7 7

strongly branched Lithothamnium tophiforme also has abundant staining bodies. However, it is not likely to occur in the British Isles, since it has not been found south of the northern Norwegian fjords. Biosystematics and ecology of epilithic crustose Cotallinaceae 357

I J I I I i I I l I l J ' I I I I L #hofhornn/um glGcl~/e L /Thothornnl~/m sonder/

-o Llthothamn/urn glaccble-Gl plants L/Thotharnn/k/rn sonder/ - 34plants

Diameter measurement: cell lumen ~ o Length: pit to pit o ep. = epithatlial or cover cell -

I I I i I I I f " o I ! I I I I i I ep. 1 2 3 4 5 6 7 8 ep [ 2 3 4 5 6 7 8 Cell position FIG. 6. Mean epithallial and perithallial cell dimensions in Lithothamnium glaciale and L. sonderi. Data: British Isles, Norway and Iceland.

The meristem and perithallial cell elongation patterns in L. sonderi and L. glaciale (Fig. 6) are quite typical of the genus (Adey, 1966b; Adey & McKibbin, 1970), and the cell dimensions are also similar to those published previously. In L. glaciale much of the cell elongation occurs in the meristem but unlike the Clathromorphum species, for example, some additional perithallial elongation also occurs. It appears that the free plants have significantly larger cells than the attached plants. The general growth pattern in L. sonderi is quite similar to that found in other Lithothamnium spp., but the cells are significantly shorter and narrower than those ofL. glaciale. Although it is possibly a character too subtle to use for the identification of single specimens, pit body diameter in L. sonderi is consistently larger than in L. glaciale.

Reproduction Asexual conceptacle dimensions for European L. glaeiale (Table III) are very close to those previously described for the species in the western N. Atlantic. Unfortunately it is very difficult to obtain adequate sections of L. sonderi Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 conceptacles and the data presented are derived from a very few specimens (Table II). The conceptacles in this species are apparently very short-lived, and, when in a mature state, are fragile and often destroyed in preparation. Carpogonial-cystocarpic development in a species of Lithothamnium has not previously been described. Although the following discussion is based on drawings of plants collected in the Gulf of St Lawrence and Newfoundland, the sectioned European sexual plants show structures that agree in every way. The sexual conceptacle primordium in Lithothamnium glaciale develops directly from the meristem between the perithallium and the epithallium, the epithallium being raised and sloughed off with upward growth of the conceptacle (Figs 7-9, 13, 14, 17, 26). No additional vegetative growth occurs on the fertile disc and the 358 W. H. ADEY AND P. J. ADEY

TABLE ]I. Conceptacle dimensions (~m), Lithothamnium sonderi

Asexual(4 concs)

C B C D Min. 160 45 I0 90

Mean 240 75 15 I10

Max. 515 115 25 125 ,4

Male (6 eoncs)

A' B C D E Min. 160 250 90 I0 45 70 8 E Mean 215 300 120 20 60 80 C Max. 295 370 160 45 70 I00 A .( > A'

Female (4 concs)

A A' B C D E Min. 145 400 115 10 7'0 35

Mean 155 410 145 30 I00 80 Max. 170 410 190 45 115 130 < ~, ,4

lateral perithallium grows centripetally to form a single-pored conceptacle (Figs 17, 26), following the pattern that is typical of the Corallinaceae. The procarp primordium is an individual meristem cell. It begins its development by enlarging, cleaving off the overlying epithallial cell and dividing off a Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 supporting cell below. The carpogonial filament initial is then cut off diagonally from the uppermost cell and this is followed by a similar production of a sterile cell (Figs 14--16). A single additional division in the carpogonial filament to form a carpogonium and a hypogynous cell, along with the marked elongation of the carpogonium to form a trichogyne, produces the mature procarp (Figs 19, 20). Complete development of procarps occurs in the central area of the conceptacle with a tendency toward incomplete development marginally (Figs 21, 27). This procarp pattern matches closely that ofLithothamnium sonderi (Suneson, 1943) and would fit into an intermediate position in Suneson's (1937) reduction series. The pattern shown for Lithothamnium intermedium Kjellmann by Masaki & Tokida (1963) shows greater reduction. However, it is not certain if the writers Biosystematics and ecology of epilithic crustose Corallinaceae 359

TABLE IlL Conceptacle dimensions (~xm), Lithothamniurn glaciale

Asexual ( 13 concs,) A BCD

Min 150 0 5 II0 Mean 245 60 25 140 Max. ::.'.360I00 40 180 < >

Male (7 concs.) ~BCDEF Min. 295 145 20 I00 0 20 Mean 360 170 50 145 25 35 Max. 430 220 70 205 65 45

< --- >

Female (3 concs.) - s_ c_ _D B Min. 295 180 135 I10 95 Mean 310 195 165 12'5 I10 , .--- Max. 325225200135 135 \

D ~ ~ Mean 455 235150200 130 75

~..~ Max. 520 320270225 180 IlO Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 intended to imply this degree of accuracy in their drawing, and it is not mentioned in the text. It is difficult to be certain of the post-fertilisation sequence of development. However, fusions of carpogonia, hypogynous cells and auxiliary cells, together with occasional fertilised procarps and supporting cells also occur. The result is a pattern of separate, scattered, irregular fusion cells (Fig. 25). Unusually large nuclei, sometimes with prominent internal staining, appear in the fusion cells (Fig. 22). Development following fertilisation must be very rapid, since few stages between those shown in Figs 22 and 24 are to be found. On a morpho- logical basis, the heavily stained cell on the upper right hand side of the fusion cell in Fig. 23 is interpreted as a gonimoblast initial which has been cut off from 360 W. H. ADEY AND P. J. ADEY

..... iII '~( ! 2

9 I0 o

Scale (,u.rn) Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIGS 7-25. Lithothamnium glaciale. FIGS 7-12. Development of male filaments. Fig. 7. Upper end of perithallial filament showing meristem cell and single epithallial cell (cover cell). Fig. 8. Sloughing off of epithallium in fertile region. Fig. 9. Primary division of primordial cell into a large celled uniseriate filament. This stage corresponds approximately with that shown for the female conceptacle in Fig. 17. Fig. 10. Development of spermatangial mother cells. Fig. 11. Early development of spermatangia. Fig. 12. Pair of mature male filaments. FIGS 13-21. Development of procarps (drawings from conceptacle centre area unless otherwise noted). Fig 13. Perithallial filament with epithallial cell. Fig. 14. Sloughing off of the epithallium and the development of a single supporting cell, an auxiliary cell and a Biosystematics and ecology of epilithic crustose Corallinaceae 361

the fusion cell. Visible attachments of the mature, two-celled gonimoblasts (sporangium and supporting cell) to fusion cells, although difficult to find, do occur (Fig. 26). A mature cystocarp is shown in Fig. 28. Although tending to occur more densely around the conceptacle perimeter, carposporangia do develop over the entire conceptacle. The upright pattern of gonimoblast development shown here is also exhibited by Lithothamnium intermedium (Masaki & Tokida, 1963) and is stated to occur in L. sonderi (Suneson, 1943). It contrasts markedly with the lateral or centrifugal type of development seen in Leptophytum. Although the final cystocarp pattern is similar to that in Phymatolithon, at least in two cases in that genus, P. polymorphum (Heydrich, 1900 ;.Rosenvinge, 1917) and P. lenormandii (Suneson, 1943 ; Adey, 1966b), fusion cells do not generally occur. The development of the male filaments in Lithothamnium glaciale is indicated in Figs 7-12. This is the only detailed pattern of male filament development described for Lithothamnium. There is a number of apparent differences in development as compared with Leptophytum laeve and Phymatolithon lenormandii (Adey, 1966b), but a formal comparison between these genera would not yet be warranted in view of the limited information available. As discussed earlier (Adey, 1965; Adey & Johansen, 1972), the pattern of male filament development in Clathromorphum is markedly different.

Mesophyllum Lemoine 1928 The genus Mesophyllum has generally been considered to be tropical (see, e.g. Johnson, 1961). However, Adey (1970a) transferred large numbers of Litho- thamnium species, which had not been re-examined since Foslie's time, to that genus. As a result, it now appears that a large percentage of the species belonging to Mesophyllum occur in the southern hemisphere, including Antarctica. Some species do extend into the northern hemisphere, but only to temperate or warmer boreal waters.

Distribution Mesophyllum lichenoides is a common sublittoral epilithic plant on the Spanish coast and extends into the Mediterranean and down the African coast (Hamel & Lemoine, 1952). In all of our collections from the southern Bay of Biscay and in Galicia it was abundant in shallow to mid-depths while at both of Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 carpogonial filament initial. Fig. 15. Enlargement of carpogonial initial and the development of a sterile cell. Fig. 16. Procarp from marginal area of the same conceptacle which bore the centre procarp of Fig. 15. Fig. 17. Developing female conceptacle: procarps at about the stage of development shown in Figs 15 and 16. Fig. 18. Procarp with hypogynous cell and young carpogonium. Fig. 19. Procarp with sub-mature carpogonium. Fig. 20. Mature procarp. Fig. 21. Reduced procarp from lateral area of conceptacle centrally bearing the procarp of Fig. 20. FIGS 22-25. Development of the cystocarp. Fig. 22. Early post-fertilisation: fusion of carpogonium to hypogynous cell and auxiliary cell; localised fusions of auxiliary cell with adjacent auxiliary cells. Note large nucleus, interpreted as diploid. Fig. 23. Gonimo- blast initial developing from fragmentary fusion cell. Fig. 24. Two-celled gonimoblasts (supporting cell and carposporangium) developed in mature cystocarpic conceptacle. Fig. 25. Horizontal section through the base of a mature cystocarpic conceptacle showing a number of irregular fusion cells. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

mr/elOOS o6z 06~ b Biosystematics and ecology of epilithic crustose Corallinaceae 363

Fie. 30. Geographical distribution of Mesophyllum lichenoides in the northern North Atlantic. Recorded as in Fig. 3. Mean of two maximum adjacent zones (epilithic specimens). X = epiphytic or British Museum specimens.

the C6te Basque stations the plant was dominant in the 3-9 m zone (Fig. 30). On the French coast, it was found epilithic only at Belle Isle. In the British Isles it was not found on rock substrate at all, althoughin many of the Channel stations it occurred epiphytically on Corallina or in debris underlying a heavy Corallina cover. Among a number of specimens in the British Museum, mostly from Corn- wall and Devon, are some from as far north as Mull. Lemoine (1923) reports the plant from Rockall, where she states, the plants were found "sur les roches". Its occurrence in the British Isles can be summed up thus: occasional in southwestern areas, epiphytic on Corallina in shallow water, probably sometimes epilithic especially in southwestern Ireland. Lemoine (1913) has reported it living unattached (rhodolith), on sand from the west of Ireland. L. M. Irvine has person- ally collected or seen herbarium specimens of epiphytic M. lichenoides from Harris in the Hebrides and from the Orkneys.

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Description of species Mesophyllum lichenoides (L.) Lemoine: Thin (100-620 ~m), "leafy" crusts with a glossy, "rolling", purple to pink surface; hypothallium thick 60-220 ~m, subparallel to substrate and coaxial; epithallium usually present, of short, wide and rounded to "rectangular" cells, 2-6 ~m long, 3.5-10 ~zm in diameter; meristem elongate, cells 2-5-12 ~m long, 2.5-7-5 ~m in diameter; perithallial growth

FIGS 26-29. Lithothamnium glaciale. Sections of conceptacles. Fig. 26. Young female conceptacle: the epithallium still closes the incomplete conceptacle aperture. Fig. 27. Mature female conceptacle. Fig. 28. Mature cystocarpic conceptacle. Fig. 29. Mature male conceptacle. 364 W. H. ADEY AND P. J. ADEY

partly progressive, seventh cell 7.5-10 ~m long, 3~,.5 Fm diameter, pit bodies very small, irregular staining bodies rarely present; (tetrasporic) asexual conceptacles raised (150-250 ~m high), cavities 420-670 Fm in diameter; cystocarpic conceptacles raised (approx. 290 ~zm high), cavities 430-600 Fm in diameter (see Table IV). (Data: France and Spain.) TABLE IV. Conceptacle dimensions (t~m), Mesophyllum lichenoides. The conceptacle height values are omitted here as vegetative upgrowth occurs and the cystocarpic conceptacles are apparently long-lived. The height shown in the drawing is typical for a young conceptacle

Asexual (5 concs.)

A B C D Min. 420 t50 60 150

Mean 520 205 85 245

Max. 670 250 130 370

Cystocarpic (3 concs,)

A B C D

Min. 450 -- 160 180

Mean 490- 175 195

Max. 600 -- 190 220

Mesophyllum lichenoides seldom offers any problems of identification. As an epilith, it has a glossy violet colour, with a smooth "flowing" texture that slightly resembles Phymatolithon polymorphum (or perhaps rarely Phymatolithon lenormandii). However, its large raised conceptacles and uplifted growing margins usually allow easy differentiation. In difficult cases, the coaxial hypothallium can Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 usually be distinguished with a dissecting microscope by careful orientation of a plant chip. The perithallial elongation curves of Mesophyllum lichenoides (Fig. 31) are very close to those previously described for species ofLithothamnium (L. glaciale, L. lemoineae, L. corallioides) and Mesophyllum eonchatum (Setchell et Foslie) Adey (Adey & Johansen, 1972). It would appear that the long meristem, with about 10-20 ~ additional elongation ofperithallial cells after cut-off, is characteristic of both of these genera. Although the epithallial cells of Mesophyllum lichenoides tend to have squarish corners in section, the very distinctive cover cell of Lithothamnium, with the square¢t base (in section) and "ears" along the upper margins (see anatomical key), does not occur. The perithallial cell lumen shows a Biosystematics and ecology of epilithic crustose Corallinaceae 365

Cell posifion ep I 2 3 4 5 6 7 I I J I I i I [

:::L8 ~7

(D 5

I I

I I ] [ ! i FiG. 31. Mean epithaUial and perithallial cell dimensions in Mesophyllum lichenoides. Data: 16 epilithic plants, France and Spain. marked decrease in diameter with cell burial. Presumably this results from increased thickening (calcification) of the cell walls. This is unusual in the crustose corallines, however, and has been previously described only in the parasite Kvaleya epilaeve Adey et Sperapani (Adey & Sperapani, 1971). Perhaps the increase in calcification permits the plant to maintain a leafy habit and enables the tissue to grow above the substrate, thereby achieving a space competition advantage. Phymatolithon Foslie 1898 The Phymatolithon species dominate the crustose coralline populations in boreal areas of the eastern North Atlantic, especially at shallow to mid-depths. This situation contrasts strongly with the shallow zones in subarctic areas where

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Clathromorphum and Lithothamnium species predominate. In more temperate waters, there is a tendency for Lithophyllum and Mesophyllum species to become the dominant groups. Distribution Phymatolithon lenormandii is primarily an intertidal species, although it can occur in considerable abundance in the 0-3 m zone (Fig. 32). In the 3-9 m zone it develops in only trace amounts and it is rarely found below 15 m (Fig. 34). In this respect, the distribution ofP. lenormandii in the British Isles is typical of its occurrence throughout the North Atlantic (Adey, 1966b, 1966c, 1968, 1971). P. lenormandii is certainly not an arctic plant. We have not found it north of New- foundland, on the north or east coasts of Iceland or in northern Norway, nor has 366 W. H. ADEY AND P. J. ADEY

FIG. 32. Occurrence of Phymatolithon lenormandii in the British Isles, 0-3 m. Recorded as in Fig. 3. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIG. 33. Geographical distribution ofPhymatolithon polymorphum in the northern North Atlantic, 0-9 m. Recorded as in Fig. 3.

it been described with certainty from the tropics. It apparently ranges from boreal to subtropical waters, but present taxonomic confusion (see, e.g. Dawson, 1960) prevents a more clear-cut geographical characterisation. Along with Phymatolithon laevigaturn, P. lenormandii tends to be especially abundant, in the intertidal and uppermost sublittoral, in areas having wide temperature ranges and somewhat lowered salinities. Probably, on the very Biosystematics and ecology of epilithic crustose Corallinaceae 367

12[ t ~ I r 6OJ I I I J 34 50JQ~ 36

30 oi<20 - I0

1 0 I0 20 30 4O 50 0 I0 20 30 40 50

12 I I I I 60 1 I I I ] 35 50 37

6 3O 41 20

2 I0 i 0 I0 20 30 40 50 0 I0 20 30 40 50 Depth (m) FIGS 34-37. Depth distributions of epilithic Phymatolithon species in the British Isles. Mean, all stations. Fig. 34. Phymatolithon lenormandii. Fig. 35. Phymatolithon laevigatum. Fig. 36. Phymatolithonpolymorphum. Fig. 37. Phymatolithon rugulosum.

limited substrate available, it is especially abundant in the southern North Sea. It seems likely that these two species penetrate farther into the Baltic Sea than other corallines but probably not to salinity levels of < 15%o. Most species of crustose corallines probably will not occur where salinities are often below 20- 24%o. Phymatolithon polymorphum apparently can withstand salinities at least down to 15%, but is probably limited in the estuarine environment in northern waters by low temperatures in winter (see Adey, 1970b) and, of course, by fine substrate. Although absent in the western North Atlantic, Phymatolithon polymorphum is the dominant crustose coralline in shallow to middle depths (Figs 33 & 36) on the European coast. In the north, it occurs at least to the Russian-Norwegian border and probably beyond (Zinova, 1955), and it has been reported from Morocco (Hamel & Lemoine, 1952). At most outer coast stations in western and northwestern Norway (Adey, 1971) and the south of Iceland (Adey, 1968), commonly 50-70 %, but sometimes up to 90 % or more, of the total area covered by crustose coralline in the shallow zones is occupied by P. polymorphum. At

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 some especially exposed stations (e.g. Espevaer and Lofoten, Norway) it is dominant to over 30 m. The northern Scottish stations generally lie within the triangle of maximum abundance of P. polymorphum (Fig. 33), where it reaches abundance values of 60-70 %. However, the Shetland station shows as a marked anomaly in a pattern that is somewhat more irregular than most species but nevertheless fairly consistent throughout the exposed northern boreal. Litho- phyllum orbiculatum and Phymatolithon rugulosum together replace P. polymorphum in the shallow zones of this station, but only L. orbiculatum could be considered to be particularly anomalous in this respect. P. golymorphum is primarily a plant of exposed coasts. In Norway (Adey, 1971) it is markedly reduced in abundance inwards along the fjords. Probably this is related to low winter temperatures in the fjords. Thus, in west, north and 368 W. H. ADEY AND P. J. ADEY

east Iceland only traces of the species are found in the most exposed areas and none was found in the fjords. Its abundance is relatively low in Loch Linnhe as compared to Copeland Island (off Belfast Lough) or the Isle of Man. Both the Cork and Welsh stations are fairly exposed and also show relatively low abundances. However, this is probably a reflection of the general reduction southwards. Phymatolithon laevigatum occurs on both sides of the North Atlantic, region- ally in rather high abundances (Fig. 38). It is especially characteristic of areas with wide temperature ranges and lowered salinities, fjords, bays, sounds and estuaries. Adey (1971) treated the plant as a subarctic species requiring winter temperatures of below 3--4°C for reproduction. However, its abundance at Cork, Plymouth and Portsmouth indicates that it can live with considerably higher winter temperatures, perhaps to 10°C, though there is the possibility in each of these cases that reproduction does not normally occur and that the populations are supported by recruitment from nearby colder bay areas. Generally, P. laevigatum is a markedly shallow water plant, with peak abundances occurring in either the 0-3 m (Adey, 1964) or 3-5 m (Adey, 1971) zones. This pattern is reflected in the British Isles (Fig. 35), but is somewhat less obvious in the data compiled for the entire area, owing to the comparative irregularity in occurrence of the species. At individual stations where it is well represented, the typical pattern is followed more closely.

ao~_ _ '" --- - ~ ~ ,o - ~ (,

NORTH ATLANTIC OCEAN ~'---o Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIG. 38. Geographical distribution of Phymatolithon laevigatum in the northern North Atlantic. Mean, 0-15 in. Recorded as in Fig. 3.

Phymatolithon rugulosum, perhaps along with Lithophyllum orbiculatum, is the most geographically widespread of North Atlantic boreal crustose corallines (Fig. 39). It occurs on both sides of the North Atlantic and like L. orbiculatum is apparently "oceanic" in character, generally occurring in abundance only at exposed or island stations. Unlike L. orbiculatum, it apparently does not compete strongly where summer temperatures are below 7-8°C. P. rugulosum, not pre- Biosystematics and ecology of epilithic crustose Corallinaceae 369

-,_ ,,, ~ ...... ,~ )" __ / - ; i

FIc. 39. Geographical distribution of Phymatolithon rugulosum in the northern North Atlantic. Mean, 3-21 m. Recorded as in Fig. 3.

viously recorded for Britain, is characteristic of middle depths in the British Isles (Fig. 37) as well as in the western Atlantic (Adey, 1964). In southern Iceland, where it apparently lacks competitors, its relative abundance in deeper water is very high (Adey, 1968). In this situation, absolute abundance data would be most valuable. Phymatolithon ealcareum is an important constituent of maerl or rhodolith deposits in the British Isles, but it is not known with certainty as an epilith. Its distribution is discussed below (Ecology). Its taxonomy, morphology and anatomy were discussed in detail by Adey & McKibbin (1970). Descriptions of species Phymatolithon lenormandii (Areschoug) Adey: Plants crustose, 40-210 ~m thick; the vegetative surface smooth to slightly irregular when young, sometimes becoming squamulose; pink-violet to violet, glossy when vegetative; hypothallium 4-10 cells, 14-75 t~m thick, with cells 8-25 ~m long, 3-11 ~m in Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 diameter; perithallial cells 1.5-12 ~m long, 3.5-10 btm in diameter; epithallium absent or a single layer of cells, meristem on surface; all conceptacles developed adventitiously from a sunken primordium 5-7 cells below the surface at centre, at maturity raised above the surrounding surface; sporangial conceptacles mostly producing bisporangia, some tetrasporangia; conceptacles crowded giving the plants a rough appearance, pore plate with 6-34 pores, 80-210 ~m in diameter, conceptacle cavity 122-267 ~m diameter, 80-138 ~m high; spermatangial conceptacle cavity 136-210 t~m in diameter, 73-122 ~m high; carpogonial conceptacles always hermaphroditic (Gulf of Maine) with at least a limited development of spermatangial clusters included, conceptacle cavities 97-145 ~m in diameter, 57-115 t~m high; carpogonial filaments developed over entire conceptacle 370 W. H. ADEY AND P. J. ADEY

bottom; carpospores apparently developed directly from small irregular fusion cells over much of the bottom excepting the central area; at maturity cystocarpic conceptacle cavities 145-275 ~m in diameter, 95-160 ~m high. (Data: western North Atlantic plants (after Adey, 1966b).)

Phymatolithon polymorphum (Linnaeus) Foslie: Crustose plants, usually one to several mm thick, but known up to 20 cm; smooth, glossy, "flowing" appearance, but, depending upon age, substrate and thickness, sometimes very irregular; colour bluish red to violet to blue-violet; hypothallium subparallel to substrate, 22-300 ~tm thick, cells 5-29 ~tm long, 3-13 ~tm in diameter; perithallium becoming very thick, upper 8 cells showing progressive elongation, the meristem cells being 1.5-8.5 ~.m long and the eighth cell being 3-5-12-5 ~tm long, cell diameters 2.5- 7.5 ~m; epithallium sometimes absent, when present cells 2-6-5 ~zm long, 3-9 ~m in diameter; all conceptacles developed from sunken primordia; tetrasporic or rarely bisporic conceptacles developing in the autumn and winter, conceptacles sunken with roofs 9-100 ~tm below the plant surface, cavities 135-225 ~m in diameter; spermatangial conceptacles with cavities 160-180 ~m in diameter, at maturity apex sunken (to 18 ~tm) or raised (to 14 ~m) relative to the plant surface; carpogonial conceptacles with cavities 155-210 ~tm in diameter, apices at maturity sunken (to 62 ~tm) or raised (to 120 ~zm) relative to the plant surface; cystocarpic conceptacles without a single large fusion cell, cavities 250-350 ~m in diameter, apices sunken (to 45 ~m) or raised (to 90~zm) relative to the thallus surface. (Data: British Isles, Norway and Iceland.)

Phymatolithon laevigatum (Foslie) Foslie: Crustose plants usually thin and ranging from about 50 ~tm to 1 mm thick, not known in massive form; surface generally smooth but often with scattered slightly raised ridges or small mounds around 1 mm across and sometimes white-edged; pink to pink violet; hypothallium subparallel to substrate, but thin, 15-55 ~zm, cells 5-22 ~m long, 4-10 ~tm in diameter; perithallium showing progressive growth, meristem cells 3-6-5 ~tm long, 3.5-6 ~zm in diameter, eighth cell 4-8 ~tm long, 3-9 ~.m in diameter; epithallium absent in 31 ~ of measured plants, when present, a single cell, 2.5- 5 ~m long, 3-5-7.5 ~zm in diameter, rarely several cells; all conceptacles with deeply sunken primordia and at maturity with a marked rim; bisporic asexual conceptacles developing in autumn and winter, at maturity roof sunken 13- 90 ~m, cavity 215-260 ~zm in diameter; mature spermatangial conceptacles with orifice 0-55 ~m above the thallus surface, cavity 125-190 ~tm in diameter; mature Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 female conceptacles with orifices 13-18 ~zm above the surface, cavities 100-160 ~zm in diameter; mature cystocarpic conceptacles with orifices 4-36 ~.m above surface, cavities 155-180 ~m in diameter. (Data: British Isles and Norway.)

Phymatolithon rugulosum Adey: Crustose plants, usually thin but ranging from about 50 ~m to several mm thick; surfaces rugulose except just before and during conceptacle production; pink to violet; hypothallium subparallel to substrate, but usually very thin, 8-50 ~m, cells 5-30 ~tm long, 2.5-10 ~m in diameter; perithallium showing progressive growth, meristem cells 2-5 ~m long, 2.5-5 ~zm in diameter, eighth cell 3-8 ~m long, 2-6 ~m in diameter; epithallium absent in Biosystematics and ecology of epilithic crustose Corallinaceae 371

31% of measured plants, when present, a single cell 1-3.5 ~m long, 4-6.5 ~m in diameter; all conceptacle primordia sunken in perithallium; bisporic asexual conceptacles developed in autumn and winter, at maturity roofs 13-68 ~tm below thallus surface, cavities 90-160 ~tm in diameter; mature spermatangial conceptacles with sunken orifices 0-18 ~tm below surface, cavity 70-100 ~tm in diameter; carpogonial conceptacles not found in Europe; one slightly raised cystocarpic conceptacle seen, cavity 270 Fm in diameter, no large fusion cell, gonimoblasts distributed across conceptacle. (Data: British Isles, Norway and Iceland.)

The appearance of each of the species of Phymatolithon varies so greatly with its ecological situation that a simple description is only of limited value. The genus itself is distinct enough to make separation from the other genera (excepting perhaps Leptophytum) relatively simple and, when several of the species occur together on a single boulder, there is little problem of differentiation. However, this rarely occurs and to identify accurately more than perhaps 70-80 % of the plants encountered requires a population approach (i.e. study of large collections). The characteristics used in the keys presented above will become more meaningful when the investigator has gained some experience with large collections. Unfortunately the population approach is often not possible using typical herbarium specimens. Even when well-preserved and from related ecological zones, samples are often too small to show several of the species together. In individual collections containing all four species of Phymatolithon found in the British Isles, the habit relationships shown in Fig. 40 were found. Although the crust ofP. lenormandii is actually the thinnest of the four species, in surface view it often appears thicker because of its irregularity and abundant raised conceptacles. The thickness commonly attained by P. polymorphum is many times greater than that ever achieved by plants of the other three species of

Thick Bluish polyrnorphurn

~lenormand//

w Q_ z r~ (.~ D 0_ l~polyrnorphurn ! 8 Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

D c) < Rrug/osum o I CO 7. I D R lenormond/i 9 Ploev/gatum [3- 0 <[ R rugulosurn <)

F laev/gotum

Thin Reddish FIG. 40. Relative colour and thickness patterns of Phymatolithon spp. 372 W. H. ADEY AND P. J. ADEY

Phvmatolithon in Britain. The colour characteristics of the different species can be quite useful, although there is considerable overlap. Plants of the same species living under different conditions can exhibit wider colour variation than that which exists between "typical" samples of the different species. Of the four species, specimens of P. lenormandii are the easiest to identify from the surface and rarely pose a problem. In the intertidal and shallow situations where it is often dominant, its purple colour and very rough surface, often sprinkled with white dots, is unique. Under the dissecting microscope it usually appears as an irregular mosaic of individual plants, an appearance that is the result of both the abundant large raised conceptacles found in the species, and the eruptive, overlapping nature of the perithallial growth. In spite of the distinctive rough surface, growing edges of the plant can be paradoxically smooth and glossy, although remaining the same characteristic colour, and often extend out- ward from the rough portions for several centimetres in rapidly growing plants. When this smooth margin is interrupted by epiphytic growth or separated from the main body of the plant by uneven substrate so that the connection is not obvious, it is possible to mistake it for another species. In P. polymorphum the surface morphology varies widely. Under favourable conditions, it develops into thick, irregular crusts on stable substrates (ledge or boulder), while on cobbles or pebbles it is generally the thickest of the plants present. In some maerls, notably in Galway Bay, it has been found living unattached, sometimes forming nodules of such extreme irregularity as to appear to be branched. Nodules taken at 25 m off North Norway were found up to 20 cm in diameter. Its typical appearance on a more or less smooth substrate is as a lush, "flowing" crust with thick, white-edged margins. The colour is not as dark as P. lenormandii. Its areal dominance in the British Isles seems to be a result of its growth rate, and its ability to envelop and grow over much of the living or dead substrate with which it comes into contact. This characteristic, plus the typical thickness of the crust and the strong furrows paralleling the edges, gives the plant a grossly irregular appearance, although the surface, when viewed under the dissecting microscope, is typically smooth. In Britain, only Lithophyllum incrustans reaches similarly massive proportions. Differentiation between these two species is not at all difficult. Even if conceptacles are absent and surface texture is in doubt, usually no more than an examination of cell size and layering on a vertically fractured surface is required (see Lithophyllum section). The regular, finely textured surfaces of Phymatolithon laevigatum and P. rugulosum, when viewed through the dissecting microscope, contrasted with the Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 gravelly appearance of P. lenormandii and the thick "rolling" nature of P. polymorphum, serve to distinguish the former two species. Typically, in P. rugulosum the surface appears as a more or less fine network of wrinkles. In general, surface irregularity in P. laevigatum is much coarser, wrinkles are deeper and more widely spaced, and patches of dead epithallial tissue are larger and more frequent. However, just before conceptacle development, both species temporarily lose this rugose or rugulose texture, becoming quite smooth and often requiring microtome sectioning for identification. After the conceptacles appear, separation of these two species is much simplified, since the conceptacles of P. laevigatum are very wide and shallow and those of P. rugulosum appear as tiny pinholes when viewed from the surface. Biosystematics and ecology of epilithic crustose Corallinaceae 373 Anatomy The anatomy of the European Phymatolithon species is generally typical of the genus: cover cells are large and hemispherical, usually in a single layer but often lacking; meristem cells are very short, and lie directly beneath the epithallium, with perithallial cells becoming gradually larger with depth; fusions and distinct pit bodies are both common. Some caution is necessary when using perithallial cell elongation patterns alone to distinguish species of Phymatolithon and Leptophytum from those of Litho- thamnium or Mesophyllum. The typical progressive elongation pattern of the Phymatolithon type is best developed when growth is actively under way. It has been demonstrated, for example, that winter elongation curves of Phymatolithon species are reduced and closer to the Lithothamnium pattern (Adey, 1964; Adey & McKibbin, 1970). Also, each species has a different potential for growth. P. polymorphum, for example, is often thick and probably has a high rate of perithallial growth. The P. polymorphum elongation curve (Fig. 41) is thus quite

I I I I I I i I 1 I /:~1 I I I I I J , i I i I I I I I /~, rugulosurn • Ioevlgoturn P, polyrnorphurn E.E(~ _ (5:3 plants) (50 plants) o (79 plants) o

~ 2

~L = -y f

o -0 I ~ E T 11 1E 1 I T I I I I I ll E I T II I I I ep I 234 5678 ep I 2545678 epl 234567 Cell position FIG. 41. Mean epithallial and perithallial cell dimensions in the major Phymatolithon spp. All areas, eastern North Atlantic. steep and strikingly different from anything to be seen in Lithothamnium or Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Mesophyllum. P. laevigatum, on the other hand is always a thin plant, even where it covers an extensive surface area. Its perithallial growth rate at maturity must be very low, perhaps often zero, and the small difference between "meristem" cell length and "mature" perithallial cell length seen in Fig. 41 reflects this situation. Staining bodies are usually exceedingly abundant in sections of P. laevigatum, scattered in P. polymorphum and absent in P. lenormandii and P. rugulosum. In a large majority of the P. laevigatum plants sectioned, great quantities of staining bodies, averaging from 1-2 ~tm in diameter, are seen in all parts of the tissue; rarely, however, otherwise typical examples of the species have been found having very few. In P. polymorphum, where the occurrence of staining bodies is noted in 374 W. H. ADEY AND P. J. ADEY

about 50 ~o of our sections, more often in the lower portions of the tissue or in scattered patches, a few cases have been seen where their abundance equals that found in P. laevigatum. Generally, the Phymatolithon species can be divided into two groups: those with massive hypothallia (P. lenormandii, P. polymorphum) and those with quite thin but still substrate-parallel hypothallia (P. rugulosum, P. laevigatum) (see Table V). In practice, the thickness of the hypothallial layer in proportion to the

TABLEV. Hypothallial cell measurements (~tm), Phymatolithon spp. Diameter Length Thicknessof layer Measurementsfrom: (number) max. mean rain. max. mean min. max. mean min. cells plants stations P. rugulosum 10 4-5 2-5 30 10.3 5 50 23.5 8 147 50 21 P. laevigaturn 10 6-2 4 22 11.9 5 55 29 15 64 22 14 P.polymorphum 13 6'3 3 29 13.9 5 300 87 22 676 75 40

whole tissue can be as useful in differentiating Phymatolithon as simple thickness. Although not thick in absolute dimensions, the hypothallium in thin crusts of P. lenormandii frequently comprises half of the total thickness of the plant, and is therefore proportionally the best developed. P. polymorphum, which varies so greatly in total thickness, can show a hypothallial layer comprising one quarter to one third of the tissue, although in thicker plants it is often obliterated by the action of borers. In these two species, the lower perithallial cell filaments curve strongly, and straight filaments, perpendicular to the substrate, are confined to the uppermost portions of the tissue. P. rugulosum and P. laevigatum, on the other hand, are plants in which the hypothallial layer does not constitute a major portion of the total tissue. The perithallial cell filaments show a greater tendency toward perpendicular orientation, the entire tissue often consisting of long vertical strands with no significant curving. However, this is often difficult to see in crusts growing on a very irregular substrate, or in those which have been made irregular by external factors. In most cases the distinction between P. rugulosum and P. laevigatum is easy to make in section because P. rugulosum is not known to have staining bodies and P. laevigatum usually has them in great abundance. P. rugulosum cells are generally the smallest of the genus, although pit bodies are larger and are prominent features in the tissue. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Where some question exists as to the separation between closely related species, multivariate diagrams can be very useful. Although time-consuming to develop, these can be employed to solve critical identification problems in a particular area. Fig. 42 was developed to separate P. polymorphum from P. rugulosurn in Iceland. There, these two species form virtually the entire epilithic coralline flora, and, although P. polymorphum is dominant in shallow water and P. rugulosum in deeper, there is a considerable zone of overlap.

Reproduction Except for the apparently non-phasic Phymatolithon lenormandii, all of the Phymatolithon species studied in European boreal-subarctic waters showed a Biosystematics and ecology of epilithic crustose Corallinaceae 375

Pit factor (Y)=de/L-5 d =nit elinrn~ter 8-0 [ I I I I I L L Tissue factor (Z) = ~. staining body occurrence 7"0

no staining ? staining few staining abundant bodies ,adies bodies staining bodiq 60 8.c Ioi 'i__ 21 irregular slightly even tissue t ' SSSue ~- ' r rt,egsUule° r 5'0 7.c 4-0

6"C O_ 30

5'C 20

4'C io Z Q. 3C

2.(

20 40 60 80 too i20 140 160 Hypothallium thickness (~m)

Data from Iceland

FIG. 42. Pit factor as a function of hypothallial thickness and tissue and pit factor-- Southern Iceland, Phymatolithon polymorphum and P. rugulosum.

marked cyclic asexual reproductive pattern (Figs 43-45). In each case, asexual primordia are formed in September or October and a large percentage of the populations bear mature asexual conceptacles by December. During the summer Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 months only vegetative plants or plants bearing degenerate conceptacles are to be found. These patterns agree closely with those previously published for P. laevigatum and P. rugulosum in the northwestern North Atlantic (Adey, 1964). The dimensional characteristics of mature asexual conceptacles of each of the species are shown in Tables VI-VIII. When conceptacles or their remains are present, species differentiation is fairly easy. P. lenormandii is the only species to have raised conceptacles typically, and these seem to be present all year in abundance. Of the species having sunken conceptacles, P. laevigatum has the largest and these develop relatively close to the surface in proportion to their width. They are often broken out and filled by new perithallial growth after spore release. Buried conceptacle cavities are not as commonly seen in section 376 W. H. ADEY AND P. J. ADEY

Month 8 9 IO 12 t 2 3 4 5 6 7

~ o ~ o--- ,°° / 75

.-~ 25

m O( m ~ 75

~> 75 ~o 5o

0 I I I I I I I 23 14 5 2 I 0 I I 2 0 2 13 No of plants sectioned FxG. 43. Asexual reproductive cycle of Phymatolithonpolymorphum in European Atlantic waters. Based on microtome sections.

in P. laevigatum as in the other species and characteristic scars indicating regrowth are often distinctly visible. P. polymorphum conceptacles are not as wide as those of P. laevigatum, and, after spore release, they are often overgrown. Filling of the cavity does not occur as often as in P. laevigatum and is frequently incomplete. Buried cavities of the same dimensions as mature conceptacles are common although sections containing none are not infrequent. Phymatolithon rugulosum conceptacles are the smallest of the group, and are formed proportionally much deeper in the tissue. Empty cavities are frequently

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 seen buried in sections of this plant. Mature male, female and cystocarpic conceptacles have been found for all of these species and dimensional summaries are also given in Tables VI-VIII. Cystocarpic conceptacles of all of the Phymatolithon species studied to date, including the P. polymorphum, P. laevigatum and P. rugulosum populations studied here, lack a distinct large fusion cell and have short gonimoblast filaments more or less uniformly scattered over the base of the conceptacle.

Leptophytum Adey 1966b The genus Leptophytum is apparently bipolar in distribution (Adey, 1970a), with some representatives, probably in deeper water, in lower latitudes. However, Biosystematics and ecology of epilithic crustose Corallinaceae 377

Month 6 z 8 9 ]0 ii 12 I 2 3 4 i i ] i i i o i i i o o e ~ 4C

• ~ 80 ~ .~ 40

® 0 =-- 9~ 40 mm

2 ~ 60

a g 40

"s o

20 o o-- u ~ 20 5°

m 20- ~o I I ~ I I I I I I I I I 6 6 6 .5 15 6 0 I 0 0 0 NO. of plonts sectioned Fro. 44. Asexual reproductive cycle of Phymatolithon laevigatum in European Atlantic waters. Based on microtome sections.

because of the difficulty in distinguishing between Leptophytum and Phymatolithon without reproductive material, their phytogeographic patterns will remain somewhat in doubt until many of the species involved can be studied in more detail. Only a single species, Leptophytum laeve, is treated herein. Another possible member of the genus, "Lithothamnium" (Phymatolithon-Leptophytum) bornetii, which was found northwards to the southernmost British Isles, is briefly discussed in the systematic list. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Distribution Leptophytum laeve (Fig. 46) is an important arctic-subarctic plant occurring primarily in the deepest photic zones, especially abundantly on shell-pebble bottoms (Adey, 1966b, 1966c, 1968, 1971). In the Shetlands station, L. laeve occurred in small amounts in the 28-37 m zone and abundantly from 37-46 m. At the outside of Loch Broom, small amounts were found in the 28-37 m zone, while on Cadial bank at the mouth of the inner loch at 21-28 m it constituted 14 % of the crustose corallines. Further south, off the northwest side of Lismore Island in Loch Linnhe, one specimen was found at 21-28 m. Two small dredged specimens were found in the British Museum collections from the Firth of Clyde 378 W. H. ADEY AND P. J. ADEY

Month 9 I0 I I 12 I 2 3 4 5 I I I I I I I I L

25 E a_ O(

I00

Q_ 75

50 l / 2~ / / 0

I00

> 25 s, e

I I I I I I I 7 2 3 I0 0 0 0 0 0 9 1.5 No. of plants sectioned FIG. 45. Asexual reproductive cycle of Phymatolithon rugulosum in European Atlantic waters. Based on microtome sections.

near Cumbrae. It was not found at the stations occupied to the south nor at the more exposed stations in the Orkneys and the Hebrides. Thus, as in Norway, Iceland and the western North Atlantic, it occurs in deeper water and strongly favours fjord-bay stations. Kvaleya epilaeve (Adey & Sperapani, 1971), a common coralline parasite on L. laeve in the north, has not been found in the British Isles.

Description Leptophytum laeve (Stromfelt) Adey: Thin crustose plants, ranging up to 650 tzm Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 in thickness; surface quite smooth, except for substrate irregularity, colour pink; hypothallium subparallel to substrate, 15-80 Fm thick, cells 10-26 Fm long, 3-5- 12 Izm in diameter; epithallium large rounded cells, 3-9 ~zm long, 6-12 ~tm in diameter, often absent; meristem cell short, 3.5-9.5 Fm long, 5.5-10.5 ~m in diameter; perithallial growth progressive, eighth cell 5-14 ~m long, 5-11 ~tm in diameter; asexual conceptacles bisporic or tetrasporic, cavity 500-680 izm in diameter, raised above vegetative surface at maturity 100-270 ~m; male conceptacles conical, raised 100-225 Fm, cavity 235-305 fzm in diameter; only one female conceptacle seen, raised 210 Fm, cavity 145 pum in diameter; cystocarpic conceptacles raised 205-370 ~m, cavity 405-590 ~m in diameter; gonimoblasts lateral. (Data: Iceland and Norway.) Biosystematics and ecology of epilithic crustose Corallinaceae 379 TABLE VI. Conceptacle dimensions (~m), Phymatolithonpolymorphum

< ,4" -> Asexual (16 concs.)

.d ,d'.4" B C D E

Min. 135 75 I00 0 I0 20 65

Mean [80 I00 155 9 50 30 115

Max 230 160 210 45 I00 45 145

< `4' > Mole (4 concs.)

Min. I60200-18 II0 25 I55

Mean t70 220 -8 120 35 155

Max. 180 260 14 140 55 180

< > Female (5 concs.)

Min. 155 27'0 -62 I00 70

Mean 190 525 55 I10 95

Max. 210 360 120 120 190

< > `4' • Cystocarpic (4 concs.)

Min. 250270-45135 115 35

Mean 315 310 50 175 175 45

Max. 350 340 90 225 300 55

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Leptophytum laeve is usually not a difficult plant to identify. Asexual or cystocarpic conceptacles, or their remains, are generally present and their large size (Table IX) serves readily to distinguish the species. In its vegetative condition, its smooth, unspeckled, pink surface usually will distinguish it from the Phymato- lithon and Lithothamnium species. In section, the perithallial ceils appear relatively large (Fig. 47), as do the rounded hypothallial cells. Staining bodies are absent.

Lithophyllum Philippi 1837 Lithophyllum has been considered a tropical genus. However, although it is generally present in a rock or coral environment in tropical to subtropical sub- 380 W. H. ADEY AND P. J. ADEY

TABLE VII. Conceptacle dimensions ([zm), Phymatolithon laevigatum

Asexual (9 concs.) A' 0 ~ ~r ~-- A /7' B C D E Min. 215 225 -5 15 20 65

Mean 235 260 7 50 30 90

Mox. 260 300 18 90 35 125

Male (G concs.)

A' A X~' B C O L2~.~/~ (~ Min, 125 190 0 90 70 Mean 170 235 25 II0 95 C Max. 190 270 55 135 II0

Female (4 concs.)

A A' S C 0 B~ < /I' > Min. t00 I35 i3 35 60

Mean 140 195 17 45 70 4, A...2 Max. 160 235 18 55 80

Cystocarpic (4 concs.)

A' B,I,. < > A A' B C O Min. 155 180 4 35 90 /l Mean I65 i85 9 40 95 Max. 180 190 1.3 45 100

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 littoral regions, it is usually not abundant. A study of Hawaiian waters in progress at the present time, for example, shows that it comprises only 10-20 Yo of the total crustose corallines from low water to 100 m. Other genera, such as Porolithon and Neogoniolithon in shallow water and Hydrolithon and Litho- thamnium in deep water, greatly predominate. In our studies now underway in Caribbean waters, we find LithophYllum in considerably less abundance than in Hawaii. Species of the genus have been reported from antiboreal to boreal waters but, in terms of percentage of species in the total coralline flora, it is most abundant in the northern temperate regions (Adey, 1970a). It has not been reported either from the high arctic or the antarctic. In the northern North Atlantic, a single species ofLithophyllum, L. orbiculatum, Biosystematics and ecology of epilithic crustose Corallinaceae 381

TABLE VIII. Conceptacle dimensions (Fro), Phymatotithon rugulosum

Asexual (13 concs.}

< ,4 ,, > <,4'> A A' A" 8 C D E Min. 90 45 70 1,5 0 14:55 c Mean 135 TO 105 30 18 22 65

Max, 160 80 160 70 40 27 90

Mole (3concs)

AA'BC D ,4' < > M in, 70 70 O 27 4;5

c Mean 90 90 I0 33 60

Max. I00 I10 18 ]36 68

occurs throughout the boreal region and extends into the subarctic. Even at the boreal-subarctic boundary, this plant can be quite abundant in a rather irregular fashion. It is interesting to note that in the northern Pacific boreal, a single morphologically similar (but taxonomically quite distinct) Lithophyllum species is of similar ecological importance (Masaki & Adey, studies in progress). This suggests a narrow niche situation which will perhaps be understood by extensive comparative study of the two oceans. \

,o ...... < %..- o<

, J_S') o Q Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

NC)RTH ATLANTIC OCEAN

FIG. 46. Geographical distribution of Leptophytum laeve in the northern North Atlantic. Mean relative abundance in %, deepest zone at each station. Recorded as in Fig. 3. 382 W. H. ADEY AND P. J. ADEY

TABLE IX. Conceptacle dimensions (~m), Leptophytum laeve

Asexual (6concs)

A B C D E Min. 500 I00 70 225 90

Mean 585 185 80 275 160

Max. 680 270 90 370 225

Male (4 concs.)

A B C D E Min. 255 I00 68 90 45

Mean 275 150 85 155 90

Max. :515 225 I00 225 170

Female ( I concs)

g]' A A' B C D E 145 4[5 210 200 I00 90

> A s,ooarO, i ,Tconcs

A A' B C D E Min. 405590205 155 170 90

Mean 500 705 270 185 260 140

Max. 590 830 570 225 360 225 ( >

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Distribution Lithophyllum orbiculatum occurs in the western North Atlantic and is widespread in eastern areas (Fig. 48). In Europe it is abundant in shallow water east of North Cape, Norway, and remains moderately abundant nearly 4000 km to the southwest in Galicia, Spain. It also has been reported from the Mediterranean (Hamel & Lemoine, 1952). Its depth distribution is more erratic than any other species (Adey, 1966b, 1971), but it is apparent on the outer Norwegian coast that, as one proceeds southwards, the maximum abundance of the species shows a tendency to occur at progressively greater depths. However, in Wales, the south of Ireland and the western English Channel, it is again most abundant in shallow water (Fig. 49). It would appear that Lithophyllum orbiculatum is "oceanic" in Biosystematics and ecology of epilithic crustose Corallinaceae 383

I I I ] I I 1 I I

~ 9 E ~ 8 ~ 7

o 6

---- 5 0 4

IIIIIIItl

i I l [ i I I I

9 5 8 xz

~ 6 u 5

4 o

:5 I I I I I I I I 1 ep I 2 :5 4 5 6 7 8 9 Cell position FIG. 47. Mean epithaUial and perithallial cell dimensions in Leptophytum laeve. Data: Iceland and Norway. that it is most abundant in areas showing the least variation between summer and winter temperatures. The outer coasts of north Norway and east Iceland, where it reaches its maximum abundance, are characterised by yearly temperature ranges of 1-8°C and 1-6°C respectively. Even in the western North Atlantic, it is Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIG. 48. Geographical distribution of Lithophyllum orbiculatum in the northern North Atlantic. Relative abundance in %, mean two zones of highest abundance. Recorded as in Fig. 3. 384 W. H. ADEY AND P. J. ADEY

-o v ~ o _ ~ ~ _

,o~e ___~56" .2 .3 2 ,e ,, o ~ 3 ,5 ~3 .o ~J"f-~'lO ,(5 -I0

-2O 9 " ,I .),, ';o )o :_ i -50 .c O -40 oo o, -- | -50

FIG. 49. Depth distribution of Lithophyllum orbiculatum on the outer European coast. Relative abundance at each station depth zone in %. most abundant in the mouth of the Bay of Fundy where the winter-summer range is approximately 1.5-10°C, the least in the western boreal-subarctic area. It occurred in all of our British stations; only in the Irish Sea, Loch Linnhe and Galway Bay was it a minor element. Lithophyllum incru~tans is the major encruster of bedrock and pebbles in tide pools and shallow water on the northwestern Spanish coast. It extends southwards at least to Cape Blanco and probably occurs throughout the western Mediterranean (Hamel & Lemoine, 1952). Ecologically it is the equivalent of the subarctic species Clathromorphum circumscripturn. In British waters, L. incrustans sometimes forms thick crusts in tidepools, especially in the south and west. In the sublittoral (Fig. 50) it is not a major element and quickly decreases in abundance with depth (Fig. 51). Specimens have been seen from Norway (the Bergen area and on the island of Froya near the mouth of Trondheimsfjord) and the plant has been described for the Faeroe Islands (Borgesen, 1902). Lithophyllum nitorum was found, at least in small quantities, at most of the Bay of Biscay stations. On the C6te Basque, where it was most abundant (to Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 24 % at 37-46 m off Castro Urdiales), it was found in mid- to deep water. In the British Isles it occurs primarily in the south at middle depths (Figs 52, 53), being found in greatest abundance (14 % of total coralline coverage) in the 3-9 m zone off the Lizard. Generally, it occurs sporadically to the north.

Descriptions of species Lithophyllum orbiculatum (Foslie) Lemoine: Plants crustose, surface usually smooth; often small and orbicular, though sometimes extensive owing to fusion of many plants; colour chalky pink to quite yellow when grown in a well lit situation; hypothallium single-layered, cells 5-18.5 Fm long, 4.5-26 ~tm in diameter; epithallium generally multilayered 2-6 cells, rarely a single layer; cells Biosystematics and ecology of epilithic crustose Corallinaceae 385

NORTH ATLANTIC OCEAN

FIG. 50. Geographical distribution of Lithophyllum incrustans in the northern North Atlantic. Relative abundance in %, mean 0-3 m. Recorded as in Fig. 3.

2-7.5 ~zm long, 2-5-8-5 ~tm in diameter; meristem cells elongate, 5-5-15~tm long, 5-5-10.5 ~tm in diameter; perithaUium cells showing some additional elongation, first cell 4-14 ~zm long, eighth cell 5-19 Fm long, 4.5-11 ~tna in diameter; secondary pits abundant, cells usually forming layers; asexual sporangia without caps (conceptacles single-pored), cavity 85-180 Fm in diameter, fully sunken, base 72-147 ~zm below surface; male conceptacle cavities 90-135 ~m in diameter, generally sunken with base 41-72 Fm below surface but sometimes with a conical

20[ I I I

o Fig. 51 ~- o 40 50 Depth (m) Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 i i i i I

gc 2.0 g~

"6 (5 Fig. 52 tO 20 30 40 5O Depth (m) FIG. 51. Depth distribution ofepilithicLithophyllum incrustans in the outer English Channel and Irish Sea. FIG. 52. Depth distribution of Lithophyllum nitorum in the British Isles. 386 W. H. ADEY AND P. J. ADEY

ikiORTH ATLANTIC OCEAN // % A. FIG. 53. Geographical distribution of Lithophyllum nitorum in the northern North Atlantic. Relative abundance in ~, mean all zones. Recorded as in Fig. 3. orifice raised up to 22 ~m high; female conceptacle cavities 80-122 fzm in diameter, sunken, base 58-94 ~m below surface, orifice sometimes raised to 28 ~zm high; cystocarpic conceptacle cavities 100-225 btm in diameter, base 94-127 ~m below surface, orifice usually raised to 54 ~m high. (Data: Norway and British Isles).

Lithophyllum incrustans Philippi: Crustose plants, but becoming massive and sometimes quite irregular; colour chalky pink to lavender, yellowish in light- exposed situations; hypothallium single layered, possibly sometimes multilayered coaxial, cells 5-18 ~zm long, 7-12.5 ~m in diameter; epithallium occasionally up to four cells but sometimes absent, cells 1.5-6.5 ~tm long, 3-8.5 ~tm in diameter; meristem cells quite elongate 5-19 ~tm long, 4.5-8.5 ~zm in diameter; first perithallial cell 5-15 ~tm long, eighth cell 5-16 ~tm long, secondary pits abundant, cells usually not forming layers; asexual conceptacles bisporic and tetrasporic, abundant, often buried in tissue, cavity 230-360 ~m in diameter, fully sunken, base 146-323 ~m below surface, central columella usually present; Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 male conceptacle cavities 90-150 ~m in diameter, generally sunken, base 44--67 ~m below surface, but usually with a raised orifice, to 22 ~tm high; female conceptacle cavities (only 2 seen) 160-210 ~zm in diameter, base sunken 99-117 ~zm, orifice to 23 ~m high; cystocarpic conceptacle cavities (only 2 seen) 250-305 ~m in diameter, base sunken 215-245 ~tm, orifice to 18 ~m high, no basal column seen. (Data: British Isles, Atlantic France and Spain.)

LITHOPHYLLUM NITORUM sp.nov. DIAGNOSIS Plantae tenues leves crustosaeque, minores quam aliquot cm diam., atque 1-2 mm crass.; colore clare roseae; epithallium plerum e unico strato cellularum latarum, interdum nullum, raro e 2 cellulis constans; cellulis 2.5-5.5 ~tm long., 5"5-13 /zm diam.; cellulae meristematis Biosystematics and ecology of epilithic crustose CoraUinaceae 387 relative breves, 2.5-9-5 ~tm long., 4.5-11 ~tm diam. ; cellulae perithalliales aliquanto longiores ut tela profundior est; prima cellula 3.5-9.5 ~m long., octava cellula 5-11 ~tm long.; 5-13 ~m diam. foveae secondariae abundantes, perithallium plerumque stratosum; hypothallium unistratum; plantae bisporicae (aut raro tetrasporicae) cavi conceptaculorum 245-385 ~m diam., apices partita elevati 70 ad 180 ~zmsuper superficiem annulo angusto distincto praediti; (conceptacula sexualia non visa).

Thin, smooth, crustose plants, not more than a few cm in diameter and one to two mm thick; colour bright pink; epithallium generally a single layer of wide cells, occasionally absent, rarely two cells, cells 2.5-5.5 ~tm long, 5.5-13 ~zm in diameter; meristem cells relatively short, 2.5-9-5 ~zm long, 4.5-11 ~tm in diameter; considerable elongation of perithallial cells with depth, first cell 3.5-9.5 ~tm long, eighth cell 5-11 ~m long, 5-13 ~m in diameter, abundant secondary pits, perithallium usually layered; hypothallium single-layered; bisporic (or rarely tetrasporic) conceptacle cavities 245-385 ~zm in diameter, partially raised apices 70-180 ~zm above surface and with a distinct narrow annulus; (sexual conceptacles not seen). (Data: British Isles, France and Spain.) Holotype: 70-10B, 10-30; Isle of Man, Port Erin Harbour, 3-9 m; deposited U.S. National Museum, coralline herbarium. Lithophyllum incrustans and Lithophyllum orbiculatum are easily distinguished from most of the northern European coralline species by their dull, chalky surface texture, which probably results from degeneration of the upper cells of the thick epithallium. Only Clathromorphum circumscriptum is similar in appearance and it is not likely that this plant extends to the British Isles (see above). Lithophyllum nitorum has a more brilliant surface appearance and is more likely to be confused with Tenarea species. It is treated separately in the discussion that follows. The colour and texture of the plant surface is useful in distinguishing between L. orbiculatum and L. incrustans. The colour of L. orbiculatum tends to be the more ruddy of the two and its surface more dry and chalky. L. incrustans has a decidedly lavender cast and a more polished appearance. Growing edges of L. orbiculatum are regular and generally thick, tending to give solitary plants a compact appearance. The growing margins of L. incrustans appear to be less firmly fixed to the substrate, and under conditions of optimum growth often turn slightly upward. Frequently, upon convergence with another plant of the species, the margins rise abruptly forming prominent ridges. This type of growth is frequently seen in intertidal pools. Difficulty can be encountered in distinguishing between these species when they Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 are old, abraded or have grown under less than optimum conditions. Although still recognisable as Lithophyllum, normal surface characteristics are frequently obliterated, and, when the conceptacles are absent, or broken out leaving cavities of similar sizes, surface features are of little use. Fortunately, the two species typically differ in their perithallial cell organisation as observed with a dissecting microscope. Cell division in L. orbiculatum normally proceeds simultaneously throughout the meristem layer, resulting in fairly conspicuous horizontal organisation, or layering, of the perithallium. Meristem cells of L. incrustans, in contrast, apparently divide in random order, and tissue organisation appears as vertical filaments, each somewhat independent of neighbouring filaments, although con- nected by secondary pits. This tissue difference is usually not difficult to see on a 388 W.H. ADEY AND P.J. ADEY

vertical surface of a chip of dried material viewed at 50-80 × with a dissecting microscope. However, in thick plants this difference may sometimes be seen only in the uppermost perithallium. Intertidal specimens of L. incrustans (or very shallow sublittoral specimens in France and Spain) sometimes exhibit an arched lower perithallial development resembling a coaxial hypothallium. Cabioch (1971) refers to it as a "faux- hypothalle". This type of development can be confused with the horizontal layering of L. orbiculatum. The "faux hypothalle" is not found in the majority of our specimens ofL. incrustans and tends to appear only in thick or leafy plants. It seems not to be a function of normal hypothallial development, but to occur in areas of rapid growth. Growing edges which converge and subsequently turn upward and grow "back to back" generally show this development, as do expand- ing margins and areas which are undergoing regrowth after damage. Often in the course of our study, especially in the case ofL. orbiculatum, plants were selected for sectioning because their surface gloss and bright colour were unusual. Upon examination of sectioned material, the tissue appeared quite typical for the species except for a scarcity of epithallial cells. It is assumed that thick layers of these cells are responsible for the characteristic "chalky" appearance of some Lithophyllum species. When this layer is depleted, perhaps because of the browsing activities of animals or other environmental conditions, the surface of the plants exhibits a more glossy appearance. L. orbiculatum has a higher average number of epithallial cells per filament than L. incrustans, perhaps related to the typical difference in surface appearance. This is further cor- roborated by the quite glossy appearance of Lithophyllum nitorum, where more than one layer of cover cells is rare. In preliminary studies, comparisons of groups of plants from similar temperature ranges indicate that Lithophyllum orbiculatum plants show a tendency to retain fewer cover cells per filament in warmer areas (Fig. 54). Measurements of L. incrustans were not available over a wide enough temperature range to make a similar comparison. From the surface Lithophyllum nitorum could be confused with the two rock encrusting Tenarea species, primarily because of the similar bright colouration. However, close comparison generally reveals L. nitorum to be more pink in colour than the violet or lavender shades of the Tenarea species. In the central part of a typical plant, cells of L. nitorurn are much smaller than those of the Tenarea species. However, in the thin growing margins they sometimes appear equally as large. Here, it is probably hypothallial cells that are being observed. Perithallial cell lengths in both of the Tenarea species are from two to four times Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 greater than in L. nitorum. This is not visible from the surface, but can be seen on a vertical section of a plant fragment. A further similarity to the Tenarea species is the strongly raised conceptacles that are present throughout the yea. However, in L. nitorum the visible portions of the conceptacle are considerably smaller, and the upper portions of the cones are always sharply demarcated from the lower. European Lithophyllum orbiculatum cell measurements (Fig. 54) are very close in every respect to those previously obtained in the Gulf of Maine (Adey, 1966b). In L. incrustans the perithallial cells are about the same length as those of L. orbiculatum, but they are significantly narrower. Perithallial cells of L. nitorum are shorter and wider than those of either of the other two species. These relationships are shown graphically in Fig. 55. The L. orbiculatum meristem cell is, on Biosystematics and ecology of epilithic crustose Corallinaceae 389

average, slightly longer than the first perithallial cell cut off and there is some additional cell elongation in the underlying perithallium. Both eastern and western Atlantic plants are the same in this regard (Adey, 1966b). The percentage of "additional" perithallial cell elongation is a little less in L. incrustans and somewhat more in L. nitorum. The meristem cell is considerably longer than the first perithallial cell only in L. incrustans.

Reproduction Without quantitative data, it was stated for the Gulf of Maine (Adey, 1966b) that "it appears that Lithophyllum (Pseudolithophyllum) orbiculatum produces its asexual conceptacles in the autumn and winter along with the Phymatolithon and

I I I I I I [ I J I & 8

L./ncrusfans 0 ( 23 plants) 7 L _ orb/cu/atum • (36 plants) 6 ~J L. n/torum & (12 plants)

4 I I I I I I I ] I J I

9 ~n 8 £ % 7 i 5

6 o~ 4 -4 5 3 Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

I I I I I I I I I I I R 3 2 I M 2 3 4 5 6 7 8 22 E E E • ¢= perithallium

Cell position Tempereture zones FIG. 54. Mean epithallial and perithallial cell dimensions in Lithophyllum spp., Atlantic coast of Europe. 390 W. H. ADEY AND P. J. ADEY

L. orb/culo/urn L. /bCfUS/ons [_, rll/oTum ep.

15 E a. 20

o 25

3O per. I c o 35

40 per.

45 c per. 5O a 55 per.

6O 65 i t'~c. 55. Graphical representation of mean epithallial and perithallial cell lumina length and diameter in Lithophyllum spp. ep. = epithallium, M. = meristem, per. = perithallium.

Month 6 7 8 9 I0 II ~2 2 3 4 I I I I I I I I I _ 4O ._o

o 20 E

"6 2C .g 0 4O m ~ 2o g

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 8O

_~ 6O

> 20

I I I -I I t I 1 B 18 13 I0 12 2 0 0 0 No. of plants sectioned I I • I I I I I 7 3 4 7 I NO. of plants sexual

FIG. 56, Asexual reproductive cycle of Lithophyllum orbiculatum in European waters. Based on microtome sections. Biosystematics and ecology of epilithic crustose Corallinaceae 391

TABLE X. Conceptacle dimensions (~tm), Lithophyllum orbiculatum

"Pore" often not Asexual (13 concs.) visible in sections 8~'--~~~ A B C D Min. 85 0 t8 55 Mean 155 8 25 90

Max. f80 22 35 120

Mote (10 concs.)

,,4 B C D Min. 90 0 13 23 B~ Mean 105 8 2:5 52 Max. 135 22 45 45

Female (Tconcs.)

,4 B C D Min. 80-9 14 31 4 Mean 100 10 28 ,$5 Max. 120 28:58 54

Cystocarpic (9 concs.)

/~ BCD ¢ Min. I00 0 22 67 '~tD~"~ Mean 150 18 31 81 J, ~ Max. 225 54 52 I00

Clathromorphum species". This statement is supported by our European data, Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 even though late winter and early spring plants were not sectioned (Fig. 56). There should be little problem in separating the three Lithophyllum species when conceptacles are present. The dimensions reported here for L. orbiculatum conceptacles (Table X) are quite close to those previously measured in the Gulf of Maine. The conceptacles of L. incrustans (Table XI), which generally show the same fully sunken form (sometimes both develop a slightly raised orifice), are 50-100~ larger in cavity diameter. Asexual conceptacles in 80~ of the L. incrustans measured showed a strong columella, while this has not been seen in L. orbiculatum. Asexual conceptacle diameter in L. nitorum (Table XII) is about the same as that in L. incrustans; however, the roofs are considerably raised, the orifice generally being 4-5 times higher above the surface than in L. incrustans. 392 W. H. ADEY AND P. J. ADEY

TABLE XI. Conceptacle dimensions (~m), Lithophyllum incrustans

/5' Asexual (14 concs.)

A BCD Min. 230 0 :36 .llO Mean. 285 21 62 145 Max. 360 45 125 210

Male (5 concs.)

x~ B C D Min. 90 0 22 22 _~C~_____~ Mean 120 13 38 37 Max. 150 22 67 50

Female (2 concs.)

BCD Min. 162 15 45 54 Max. 208 25 45 72

,4 Cytocarpic (2 concs )

/~ B C O Min. 250 0 58 125 Max. 305 18 68 130

.4 Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

Tenarea Bory 1833 Distribution The epilithic members of the genus Tenarea (Dermatolithon) are ubiquitous in the tropics and sometimes they are even minor "rock" builders. However, they are usually not areally dominant. Occurrence becomes increasingly rare with increase in latitude and they are absent in polar waters (Adey, 1970a). Two species extend into British waters, one even reaching southernmost Norway. Tenarea confinis was found only in the southernmost British Isles, occurring intertidally and subtidally from low water to a maximum of 9 m (Figs 57, 58). Tenarea Biosystematics and ecology of epilithic crustose Corallinaceae 393

TABLE XII. Conceptacle dimensions (~tm), Lithophyllum nitorum

Asexual (6 concs.)

< A' > A' B C D M[n. 255 555 "fO 22 100

MeQn 505 405 95 40 120

Max. 585 590 180 54 135

A Male (2 concs.)

A B C O Min. 90 18 22 22 c Mox. 118 18 22 22

hapalidioides occurs primarily at greater depths and was found at most of the British stations as well as in southwestern Norway (Figs 59, 60).

Descriptions of species Tenarea confinis (Crouan frat.) comb. nov. : (Melobesia confinis Crouan frat. 1867, Florule du Finist6re, p. 150.) Thin, violet or purple-red plants sometimes becoming extensively imbricate; hypothallium a single layer of arcuate cells 17-110 ~m long, 7.5-19 ~zm in diameter perithallium up to 5 cells thick in an individual plant, cells 16-50 ~zm Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

~'~ORTH ATLANTIC OCEAN

FIG. 57. Geographical distribution of Tenarea confinis in the northern North Atlantic. Mean relative abundance, 0-9 m. Recorded as in Fig. 3. 394 W. H. ADEY AND P. J. ADEY

1.0 I I I I I

~o~ 0.5

i Fig. 58 r~ 0 I0 20 30 40 50 Depth (m)

[ I I I [ E

Fig. 59 Depih (m) FIGS 58, 59. Depth distribution of Tenarea species in the British Isles. Fig. 58. Tenarea confinis. Fig. 59. Tenarea hapalidioides.

long, 5-14 ~zm in diameter, abundant secondary pits; epithallium typically a single layer of flattened, ovate cells 3.5-7 ~zm long, 5-12 ~m in diameter; only bisporic asexual conceptacles encountered, cavities 205-390 ~zm in diameter, apices 50-225 ~m above the surrounding thallus; occurring in lower intertidal or uppermost sublittoral. (Data: British Isles).

Tenarea hapalidioides (Crouan frat.) comb. nov. : (Melobesia hapalidioides Crouan frat. 1867, Florule du Finist6re, p. 150.) Thin, pink to pink-orange plants occasionally imbricate but usually somewhat Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIG. 6(I. Geographical distribution of Tenarea hapalidioides in the northern North Atlantic. Mean relative abundance (~) in all depth zones. Recorded as in Fig. 3. Biosystematics and ecology of epilithic crustose Corallinaceae 395

smooth; hypothallium a single layer of rectangular cells (occasionally arcuate) 12.5-70 ~zm long, 8-20 Fm in diameter; perithallium up to 18 cell layers thick, cells 12.5-50 ~tm long, 9-15 Fm in diameter, secondary pits abundant; epithallium usually a single layer of rounded cells 2-5-5-5 Fm long, 8-14 Fm in diameter; only bisporic asexual conceptacles encountered, cavities 405-540 Fm in diameter, apices 110-225 Fm above the surrounding thallus; occurring from upper sublittoral to deep water. (Data: British Isles and Norway.)

From the original Crouan descriptions of Melobesia confinis and Melobesia hapalidioides, it is not possible to ascertain the species or even the genus that was being described. The descriptions of Dermatolithon hapalidioides (Crouan) Foslie (1901, 1906), Heydrich (1900), Lemoine (1913) and Hamel & Lemoine (1952), closely resemble our concept of T. hapah'dioides. However, it appears that our T. confinis was also included by these authors in Dermatolithon hapalidioides, generally being treated as f. (or var.) confinis. Foslie (1906) indicates that the species also occurs in the intertidal, where it tends to be imbricate; Hamel & Lemoine (1952) refer to var. confinis as imbricate; Lemoine (1913) states that D. hapalidioides occurs on rocks in the littoral region where it is more violet (presumably than the typical rose, rose-red colour) (Hamel & Lemoine, 1952). In the British Isles the genus Tenarea is easily recognised by its bright colour, large raised single-pored conceptacles and large cells, visible even at 10-15 × magnification. The only other species encountered in this area which shares these characteristics is Lithophyllum nitorum, as has been discussed above. Of the two Tenarea species, T. confinis generally has a violet or violet-red colour, while T. hapalidioides has a brilliant pink-orange colour that remains on poorly dried specimens even when the colour of the other corallines present has faded. T. confinis often overgrows itself, although this is not usually apparent from the surface, and in the lowermost intertidal it can develop an irregularly imbricate surface by such overgrowing. In section, the most striking difference between the two plants is hypothaUial cell height. T. confinis has long arched cells that are generally more than twice the length of equivalent cells in T. hapalidioides (Fig. 61). Some care must be

~00 "-7 ~,t I I I I I i r

Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 ~ 7o ~ 6o

6 @ 50 ro 4o ~ 30 Tenarea hapalidio/des ~E -r- 20

I0 I I I I I I I 200 250 300 350 400 450 500 550 Asexual conceptacle cavity diameter (/zm) FIG. 61. Hypothallial cell length as a function of asexual conceptacle diameter in the epilithic Tenarea species of southwestern Europe. Data: British Isles, France, Spain. 396 W. H. ADEY AND P. J. ADEY

13 J l I l 1 1

o IC ~5~9 /1 1 I [ ~ 1 I I 3O

"~ 25 ::k ~ 20

z 10

F/G. 62. Mean epithallial and perithallial cell dimensions in Tenarea confinis (A)and Tenarea hapalidioides (O). Data: British Isles, France and Spain. exercised with small fragments, however, as occasional hypothallial cells in T. hapalidioides can be as long as the mean length in T. confinis. This condition occurs especially where there is a sharp drop or rise in the level of the substrate. The mean perithallial cell length in T. confinis is also greater than in T. hapalidioides (Fig. 62), though the difference is not marked and certainly could not serve for routine indentification of individual specimens. No consistent cytological differences have been recorded. In both species, only bisporic asexual conceptacles were encountered. These are typical for the genus, with a persistent columella present at maturity. Although

TABLE XIII. Asexual conceptacle dimensions (~tm), Tenarea hapalidioides and T. confinis.

Tenarea hapalid/o/des (7 cons.)

Min. 405450 I10 40 I00

D Meon 460 660 140 70 140 Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 "// '~/ \\-- J A' Max. ,540 8,0 225 90 [80 :)

Tenfea confi~q/$ ( 7 cons, )

A A' B C D 8 Min. 205 270 50 23 90

D Mean 270 395 I30 43 I45

Max. =J90520225 68 225 < ). ,zl' < > Biosystematics and ecology of epilithic crustose Corallinaceae 397

the height and degree of projection of the conceptacles is virtually the same for both species, the diameter of T. hapalidioides conceptacles is considerably greater than that of T. confinis (Table XIII). Because of their relatively limited abundance, crust thinness, and the consequent difficulties of preparation, our available information for these species is considerably less than for the Phymatolithon, Lithothamnium or Lithophyllum species. The basic differences appear to be well marked (see also Fig. 61), but our collections are not adequate firmly to establish whether the differences in the two populations are environmentally or genetically induced. However, our experience with crustose corallines indicates that within a species the differences in anatomy and reproduction attributable to depth are considerably more subtle than those found here. Furthermore, it is possible that T. confinis, as we have treated it, consists of more than a single species. However, we cannot establish this without a careful study of more southern populations.

FoslieUa Howe 1920 Distribution Species of this genus are ubiquitous as epiphytes in shallow water, both on marine vascular plants and other algae. A few species are epilithic in habit but there is little previous work on these because of the difficulty in collecting and removing them for sectioning. This genus rarely forms a large part of the epilithic coralline flora and was not found at all in the western North Atlantic. In the European boreal one species, Fosliella tenuis sp. nov., is widespread (Fig. 63), though usually in very small amounts. Fosliella valida sp. nov., is a Lusitanian species, more common in the southernmost British Isles (Fig. 65).

/ / -. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

NORTH"~-.ATLANTIC.....~ OCEAN~__~ ,~

FIG. 63. Geographical distribution of Fosliella tenuis in the northern North Atlantic. Mean relative abundance, all depth zones. Recorded as in Fig. 3. 398 W. H. ADEY AND P. J. ADEY

5 t I I I I 4

0 I 0 20 30 40 50 Depth (m)

FIG. 64. Depth distribution of Fosliella tenui; in thc British Isles.

Descriptions of species Melobesia (Fosliella) trichostoma Rosenvinge (1917), described from a shell in Limfjord, Denmark, is similar vegetatively to Fosliella valida; however, the conceptacles in F. valida are considerably smaller than those described by Rosen- vinge. Fosliella tenuis is dimensionally close to Melobesia (Fosliella) minutula (Foslie, 1906) but, in addition to being epilithic, F. tenuis plants are more or less orbicular rather than irregular. Thus, even though the available information is somewhat limited for these plants, we have chosen to treat them as new species. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FIG. 65. Geographical distribution of Fosliella valida in the northern North Atlantic. Mean relative abundance, all depth zones. Recorded as in Fig. 3.

FOSLIELLA TENUIS sp. nov. DIAGNOSIS Plantae tenuissimae, ubique fere pellucidae, colore dilute violaceae; crustae vegetative solum ex hypothallio epithallioque constantes; hypothallium unistratum, cellulis 8"5-18"5 tzm long., 8-16 t~m diam., cellulae epithalliales 4'5-6.5 ~m long., 4.5-6"5 ~tm diam.; trichocyta rara, cavi conceptaculorum asexualium 105-135 ~tm diam., 45-65 tzm alt., tetrasporici, unus cavus con- ceptaculi masculi 30 Izm diam., 35 ~m alt.; cavi conceptaculorum carposporangialium 70-110 ~tm diam., 35~,0 ~tm alt. Biosystematics and ecology of epilithic crustose Corallinaceae 399

Plants extremely thin, nearly transparent throughout; colour light violet, crusts consisting vegetatively of only hypothallium and epithallium; hypothaUium single-layered, cells 8.5-18.5 ~m long, 8-16 ~tm in diameter; epithallial cells 4.5-6.5 ~zm long, 4.5-6.5 ~m in diameter; trichocytes rare; asexual conceptacle cavities 105-135 ~zm in diameter, 45-65 ~zm high, tetrasporic; one male conceptacle cavity 30 ~tm in diameter, 35 ~m high; carposporangial conceptacle cavities 70- 110 ~m in diameter, 35-40 ~m high (see Table XIV). (Data: British Isles and Norway.) Holotype: 67-16, 50-70E; outer Oslo Fjord, off northeast side of Bustein Island, 8/1967; deposited U.S. National Museum, coralline herbarium.

TABLE)(IV. Conceptacle dimensions (~.m), Fosliella tenuis

Asexual (3 cones.)

A B C Min. 106 45 Mean 120 33 57 Max. 135 63

Mate (I conc)~

A B C 32 :57 I0 E-O <~

Cystocorpic ( 3 concs.)

A B C Min. 72 18 35

Mean 90 27 37 Max. 108 40 38 Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

FOSLIELLA FALIDA sp. nov. DIAGNOSIS Crustae tenues, usque ad plures quam octocellulas crass., pellucidae solum ad margines; colore roseo-aurantiaceae; hypothallium unistratum, cellulis 7-14 ~tm long. ; 5-9.5 ~tm diam. ; cellulae perithalliales 3.5-8.5 ~tm long., 2-5-6-5 ~tm diam., epithallium ex uno, raro duobus stratis constans, cellulis 2-5-5"5~zm long., 3-8 ~m diam. ; trichocyta rara; conceptacula asexualia tetrasporica unum porum habentia, depressa, cavis 75-100 g.m diam., 35-50 ~tm alt.; conceptacula spermatangialia, caves depressa 45-55 ~m diam., 25-30 ~m alt. ; conceptacula cystocarpica depressa, 75- 95 ~tm diam., 27-32 ~m alt.

Crusts thin, to greater than eight cells in thickness, transparent only at margins; colour pink-orange; hypothallium single layered, cells 7-14 ~zm long, 5-9.5 400 W. H. ADEY AND P. J. ADEY

~zm in diameter; perithallial cells 3.5-8.5 ~zm long, 2.5-6.5 ~tm in diameter; epithailium one, rarely two layers, cells 2.5-5.5 ~m long, 3-8 Fm in diameter; trichocytes rare; asexual conceptacles tetrasporic, single pored, sunken, cavities 75-100 ~m in diameter, 35-50 Fm high; male conceptacles, sunken cavities 45-55 ~zm in diameter, 25-30 Fm high; cystocarpic conceptacles, sunken, 75-95 Fm diameter, 27-32 ~m high (see Fig. 66 and Table XV). (Data: British Isles.) Holotype: 70-2, 10-30C; off Plymouth, England, Rame Head, 11/1970; deposited U.S. National Museum, coralline herbarium. Although widespread in the European boreal, especially on the Norwegian coast, the very small, thin, light violet crusts of Fosliella tenuis are often over- looked in fresh collections. The plants occur frequently in moderately deep water, appearing to be early colonisers of newly available substrate. They grow rapidly in area rather than thickness, and apparently become reproductive at a very early age. The species does not appear to be able to survive in direct space competition with other crustose coraIIines; on substrate that has been part of the environment

I I I I ] I r I r

7-- I J I J I [ i I [

ep 1 2 3 4- 5 6 7 8 Cell position Fie. 66. Mean epithallial and perithaUial cell dimensions in Fosliella valida. Data: British Isles, France and Spain.

for long enough to be largely encrusted with corallines, F. tenuis plants are found only around the periphery. Conceptacles are usually abundant, also indicating a rapid succession of populations. In Norway, F. tenuis is more characteristic of moderately deep water (27-37 m). The depth curve for the British Isles (Fig. 64) is irregular but indicates a similar pattern. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Fosliella valida is a quite well developed member of its genus; it sometimes has a lightly rugulose surface which could, superficially, be mistaken for Phymato- lithon rugulosum. However, on closer examination, its orange-pink colour and transparent margins should prevent such an error. In vertical section, its single- layered hypothallium and multilayered perithallium with abundant cell fusions will separate F. valida from any of the other species in this region. The perithallium is strikingly zonate in this species. ECOLOGY The procedures used in these studies to obtain the quantitative relative abundance data for rocky bottoms were described in earlier papers (Adey, 1966b, 1968, Biosystematics and ecology of epilithic crustose Corallinaceae 401

TABLEXV. Conceptacle dimensions(~tm), Fosliella valida

Asexual (6 concs.)

A B C Min. 75 5.5 12

Mean 87 66 14

Max. I00 77 16 < > A

Male (5concs.)

B C

Min, 47 12 25 Mean 53 15 27

Max. 57 17 .30

Cystocorpic (3 concs.)

A B C Min. 77 I0 27

Mean 89 15 30

Max. 95 15 .32

1971). Absolute abundance data, expressed as the proportion of area of bottom covered by each species, would certainly be more desirable than coverage relative to other species; however, these would be difficult to obtain on a broad geographic basis within the framework of existing funds and facilities. Zones where total crustose coralline coverage of the bottom is estimated to be less than 10-20 ~ are not included in the data, since these cases are likely to present problems in assess- ing relative abundance. As mentioned earlier, areas of maerl or unattached branching coralline were not treated quantitatively in this study. Only four such stations were occupied in the British Isles: Orkney-Pierowall Road; Scotland-Loch Linnhe; English Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 Channel-off Falmouth; Galway Bay-Doorus Strait. Specimens in the British Museum and Robertson material on loan from Glasgow Museum from the Firth of Clyde, and Galway University College material from Kilkiernan, have been examined. Adey & Macintyre (1973) have presented a discussion of the occurrence of rhodoliths (including maerl and "free" coralline). In general, because of relatively high turbidities of British waters, rhodoliths are to be expected only on flat bottoms in semi-protected bays, estuaries or archipelagos, where the lack of heavy wave action allows their development in spite of a slow growth rate (see Adey & McKibbin, 1970), but where sufficient local sea, refracted swell or current remains to prevent their burial by fine sediments. Their occurrence can be expected from 1-20 m, varying greatly with exposure. Fig. 67 shows 402 W. H. ADEY AND P. J. ADEY

NORTH A~ANTIC OCEAN " ~"~ Area of ocuc rrence of rhodolltes , . ~,

P~ymo,o,,~..~,~#~Zm ]',lill!ll - - " - ..... J -o

Jm. coral/o/des FIG. 67. Geographical distribution of main rhodolith species in the northern North Atlantic. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016

NORTH ATLANTIC OCEAN ~L Clothrornorphum corn#octurn~ Leptophytum foecundum T ...... y L/thotharnn/um toph/7orme I Most arctic~ Kvaleya ep/laeve l -~ .... Clathromorpham circurnscrlptumI -~ /~ \ Leptophy/um laeve I Most southern Lithotharnnium qlaciale

FIG. 68. Southern limits of arctic-subarctic species. Note that the designation "most arctic-most southern" is not necessarily equivalent for both sides of the North Atlantic, although it is nearly so. For example, the "most arctic" species in the western Atlantic is Lithothamnium tophiforme; in the eastern Atlantic, it is Clathromorphum compactum. Biosystematics and ecology of epilithic crustose Corallinaceae 403

-oo

--I-2

4-? z NORTH ATLANTIC OCEAN over$'~ o~r Phymatolithon calcareum~m~ ~ "~ Lithophyllum /?Tcrustans T Most northern ~ L#¢hothammum corall/o/?/esi "~~---.... "iI, L/?hophyllum n/forum ] ...... ~ ...... _ ) Tenarea confm/s i ..... Mesophyllum lichens'des i FoMiella vah~fa / Most temperate L/Thophyllum tor/uosum T

FIG, 69. Northern limits of Lusitanian species (southern elements) in the northern North Atlantic. Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 c.Q~ / ......

NORTH Phymotolithon polymorphum Phymatolithon rugulosum Lithophyllum orbicula/um Lithothomn/um sonderi Phymalolithon laev/gatum k .t.t :2 Tenarea hapalidioids Foshella tenuis FIG. 70. Limits of boreal species in the northern North Atlantic. 404 w. H. ADEY AND P. J. ADEY

the species expected to be the primary rhodolith builders in the boreal to arctic North Atlantic. Except for the wide-ranging Phymatolithon lenormandii, the crustose corallines occurring in the North Atlantic can be divided into three groups: arctic-subarctic species, occurring significantly in northern Iceland, the north Norwegian fjords, and the Arctic (Fig. 68); Lusitanian species, occurring abundantly in France and Spain and not extending northwards of southwestern Norway (Fig. 69); and boreal species, those occurring primarily in the British Isles or southwestern Norwegian areas and widely over the western European coasts (Fig. 70). This terminology corresponds with that of Adey (1971), except that Phymatolithon laevigatum is here treated as boreal rather than subarctic. The subarctic element is poorly represented in the British Isles, with only two species present, Lithothamnium glaciale and Leptophytum laeve. Lithothamnium glaciale is extremely abundant in subarctic areas such as Newfoundland, northern Iceland and the north Norwegian fjords. Although most abundant at middle depths, it even extends into intertidal pools in some places. In the British Isles, it can be important in localised rhodolith areas in bays, especially in the western Scotland sea lochs, but also occurs in pools in eastern Scotland and northeastern England (though in much less abundance than Phymatolithon polymorphum and P. lenormandii). It apparently does not occur as far south as the English Channel. Leptophytum laeve, although highly abundant in deep water to the north, was only found in abundance in deep water in the Shetlands. To the south it is a more or less rare element of the west Scottish flora. The Lusitanian element, on the other hand, is extremely important in the flora, accounting for about one-half of the species in the southwest. However, it is reduced northwards, and entirely confined to shallow water in the British Isles. In summary, the crustose coralline flora of the British Isles is primarily boreal, with a strong overriding element of Lusitanian species extending throughout and a weak element of subarctic species primarily underriding from the north. Frequent attempts have been made in the course of the study of North Atlantic coralline algae to correlate plant anatomy with environmental conditions. Adey & McKibbin (1970) demonstrated that both Phymatolithon calcareum and Litho- thamnium corallioides develop larger perithallial cells in the winter than in the summer. Plants of Phymatolithon laevigatum and Phymatolithon rugulosum (and possibly Clathromorphum compactum) develop larger hypothallial cells in deeper (and generally colder) water (Adey, 1964, 1965). In the present study, hypothallial cell dimensions (length and diameter) were Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 taken from sections of material collected at stations in Iceland, Norway, Britain, France and Spain. Within each species studied, the plants used were subdivided into groups from areas having a similar annual surface temperature range (temperature variation related to depth of collection was not considered). Since accurate temperature figures were not available for many localities, approxima- tions were sometimes necessary. For each temperature group, the sectional area of measured hypothallial cells was calculated and averaged, and the mean yearly maximum and minimum temperatures determined. The results are shown in Fig. 71. The data plotted are temperature indices (~/Tma,, "Train) as a function of mean cell area for each group. In agreement with previous studies which found smaller cells occurring at Biosystematics and ecology of epilithic crustose Corallinaceae 405

140

120

~" I00 E :t

× 80 -,j

40 |

2 4 6 8 10 12 {4 16

Ternperoture ¢/(Trnex)(7=min) (°C)

FIG. 71. Relationship between temperature and hypothallial cell size in several crustose corallines in European waters.

higher temperatures, there were general reductions in cell-sectional areas of the hypothallial cells as the temperature index increased in the Phymatolithon and Lithothamnium species studied. However, the opposite is true of Lithophyllum orbiculatum, the only species studied that has a single-layered hypothallium and belongs to the Lithophylloideae. It would be most interesting to compare this result with other major Lithophyllum and Tenarea species; however, although we have considerable anatomical data from Lithophyllum incrustans, measurements from plants collected over a sufficiently wide temperature range are not yet available.

ACKNOWLEDGEMENTS Many people have helped us in the course of this study; unfortunately it is possible here to Downloaded by [UNAM Ciudad Universitaria] at 12:15 23 June 2016 mention only the most important of these. Mrs Linda Irvine arranged the study of the British Museum material and assisted in in- numerable ways in getting through a large mass of material in the short time available. She was also responsible for arranging a large part of the field trip of November-December 1971 and later offered many important suggestions on the development of the manuscript. Dr Mary Parke arranged for the work at the Plymouth Marine Biological Laboratory and Dr Gareth Jones and Mr W. F. Farnham assisted in occupying stations from Portsmouth Polytechnic's Hayling Island Marine Laboratory. Work in both of these areas was greatly facilitated by my diving and working companion, Mr R. L. Fletcher. Dr Joanna Jones arranged for the laboratory space and joined me diving to obtain collections from a station off the Isle of Man. Professor Knight-Jones, Swansea University, with considerable effort arranged the dive in Pembrokeshire and the laboratory space at Dale Fort Field Centre. In addition to Mrs Linda Irvine, Dr Mary Parke, Prof. Peter Dixon and Dr Graham Elliott read the manuscript and offered many valuable suggestions for its improvement. 406 W. H. ADEY AND P. J. ADEY

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