W. H. ADEY Division of Paleobotany, U.S. National Museum, Washington, D.C. 20560 I. G. MACINTYRE Division of Sedimentology, U.S. National Museum, Washington, D.C. 20560
Crustose Coralline Algae: A Re-evaluation in the Geological Sciences
ABSTRACT Therefore an understanding of crustose coral- line taxonomy and habitat preferences is The crustose coralline algae are well known critical to quantitative ecological and pale- in shallow tropical waters as reef frame-builders oecological studies. This paper is intended to and sediment producers. Although their abun- develop a "fresh start," realistic viewpoints, dance at greater depths and in arctic waters and even an optimism toward the crustose has been previously recorded, this knowledge corallines in the geological sciences, where con- in recent decades has been largely ignored by siderable confusion prevails. geologists and marine scientists in general. Much of the existing confusion concerning Many erroneous or misleading ecological and the crustose coralline algae stems from either paleoecological statements and conclusions a misunderstanding of terminology or a general have resulted, and we have endeavored to failure to consider the wide generic and specific clarify matters through the citation of the older variation within the group. Perhaps more literature along with more recent ecological serious are the widely held misconceptions studies. about habitat, which can lead to wholly A parallel tendency to "simplify" the erroneous paleoecological conclusions. taxonomic structure of crustose corallines has As a result of these problems, many scientists threatened to add considerable confusion to are reluctant to undertake detailed studies modern marine studies. We have discussed involving the crustose corallines. Their in- recent work on anatomy, reproduction, and creasing frustration is well illustrated in the taxonomy. These and classical data are sum- following statements: "It is doubtful whether marized in the form of keys and an evolutionary the genera of crustose melobesioids can be tree, which are intended to provide the geo- differentiated in the field" (Marsh, 1970); logist and marine biologist with a working and, "Because most of these algae resemble facility with the group. each other so closely in their appearance, A number of quantitative ecological studies habitat requirements and their roles as herma- treating crustose corallines have appeared types, we have combined them for sake of during the past decade; these results are dis- convenience into an artificial group called the cussed and possibilities for future ecological lithothamnioid algae" (Goreau, 1963). Identi- work indicated. The occurrence of rhodoliths fications in the field are possible, however, and (maerl, free corallines) and the factors con- it has been shown that quantitative ecological trolling the development of these deposits are studies also can be accomplished both in also noted. northern waters (Adey, 1971) and in the tropics (Littler, 1971; Adey and W. T. INTRODUCTION Boykins, in prep.). The crustose corallines, which form three subfamilies (Melobesioideae, Lithophylloideae, MISNOMERS AND and Mastophoroideae) of the family Coral- MISUNDERSTANDINGS linaceae (Adey and Johansen, 1972), play Present-day problems concerning classifica- a major role in the ecology and development tion of the crustose corallines originated in the of most photic hard bottoms as well as some early 19th century when the term Nullipore sediment bottoms throughout the world. was applied loosely to crustose corallines and
Geological Society of America Bulletin, v. 84, p. 883-904, 31 figs., March 1973 883
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superficially similar animals. Later, even up Some attempts, however, have been made to to the present, all crustose corallines frequently clarify the terminology. The ridge on Raroia "pass[ed] under the widely inclusive generic Atoll in the Pacific, for example, was described name 'Lithothamnion' " (Howe, 1912, p. 839), as an "Algal Ridge" rather than "Litho- or "lithothamnioid algae" (Goreau, 1963). thamnion Ridge" because ". . . the dominant Lithothamnium (correct spelling), however, is coralline is Porolithon onkpdes not Lithotham- primarily an arctic genus; in the tropics, it is nion' (Newell, 1956, p. 344). A subsequent dis- common only in deep water. Recently, there cussion of the "Lithothamnion Ridge" misno- has been a trend to call crustose corallines "the mer indicated tha: in the tropical Pacific these melobesioid algae" (Lee, 1967), but this term ridges are constructed mainly by species of the also leads to further confusion. In fact, it genus Porolithon, and that "species belonging refers to only the typically arctic-antarctic to the genus Lithothamnium are seldom pres- Melobesioideae of the three crustose coralline ent" (Johnson, 1961, p. 25). More recently, it subfamilies. was suggested that these algal ridges have a Crustose corallines generally have been rather simple crust ose coralline assemblage be- considered shallow-water tropical organisms cause only two gsnera, Porolithon and Neo- goniolithon, were reported on the reef flats of (see below), but various species and genera are Rongelap Atoll, Marshall Islands (Lee, 1967). known to occur from the tropics to the polar Collections from reef flats on Bikini, Guam and regions. Perhaps crustose corallines are most Palau, however, show a greater variety, in- important in the polar regions where they are cluding considerable numbers of Lithophyllum commonly the main calcifiers, particularly mollucense and Lithophyllum kotschyanum (J. on hard bottoms. Also, their depth of occur- H. Johnson collections in the U.S. Geol. Sur- rence ranges from the intertidal to the lower vey; Adey, unpub.). Although upper Tertiary limit of the photic zone. In addition, a strong and Pleistocene collections of crustose coral- specific depth zonation has been observed in lines from Saipan (johnson, 1957) contained a northern waters (Adey, 1966a, 1968, 1971); number of species of Lithothamnium, at least in the tropics, depth zonation appears to be some of these belong to Mesophyllum (Adey, on the generic level (Adey, 1966b; Adey and personal observation), and no paleoenviron- W. T. Boykins, in prep.). mental data v/ere given. Recent shallow-water Lithothamnion Ambiguity plants in the same study included species of Porolithon, Neogonhlithon, Lithophyllum, and The consistent use of Lithothamnion as a Lithoporella (Lithothamnium was not reported). generic term for all crustose corallines has given rise to ambiguous terminology. One A shallow-water ''Lithothamnion'' bank was result is that the spectacular growth of crus- reported to have b:en constructed by Meso- tose coralline algae which form wave-resistant phyllum (Lithothamnion) erubescens off Bonaire ridges in many Pacific reefs were named in the Caribbean (Zaneveld, 1958). This "Lithothamnion Ridges." The ridge on Bikini identification may b; questioned, particularly Atoll, for example, was said to be "conposed as anatomical data were lacking and Neo- mainly of pink and dark-red Lithothamnion' goniolithon strictum occurs abundantly in simi- (Tracey and others, 1948, p. 867). Kuenen lar environments. In fact, recent collections (1950, p. 421-422) stated: "Most important from the Caribbean area show a general are the family of red algae called Coralliraceae, absence of the Melcoesioideae. Shallow-water generally termed nullipores, encrusting coral- (to 15 m) reef collections from Jamaica (Adey, lines or Lithothamnium. But other genera., such unpub.) consisted of 41 percent Neogonio- as Lithophyllum and Archeolithothamnium, are lithon, 25 percent Porolithon, 12 percent Litho- also of importance." Later, the algae on some phyllum (the remainder being about equally Pacific ridges were described as "encrusting divided among Arctieolithothamnium, Litho- calcareous algae 'Porolithon and other litho- porella, Hydrolithon, Heteroderma, and Lepto- thamnia' " (Ladd, 1961, p. 705). During an phytum. In deeper water (>27 m), Hydrolithon investigation of the Great Bahama Bank in the (45 percent) and Lithoporella (22 percent) Caribbean area, Newell and Rigby (1957, p. were the major elements. Another shallow- 47) noted that "a well-defined algal rim is water collection, patcii reef and lagoon, from lacking, but encrusting Lithothamnion is con- the southeastern Bahamas (Adey, unpub.) in- spicuous over the shallowest part, or crest, of cluded three species of Porolithon, two species some of the reefs." each of Neogoniolithon and Tenarea, and one
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species each of Lithophyllum and Heteroderma. and Curray, 1956; Menzies and others, 1966). Archeolithothamnium is, however, important Algal balls from a bank off the Canary Islands, below 30 m in the Bahamas and the Virgin however, were found to contain algae of the Islands; also, a Lithothamnium and a Mesophyl- genera Goniolithon and Porolithon, and were lum species occur cryptically in small amounts referred to as oncolites (McMaster and Cono- in shallow water. Lithothamnium occidentale has ver, 1966). The term oncolite properly refers been described in shallow water in Bermuda to spheroidal forms of algal stromatolitic struc- (Bosellini and Ginsburg, 1971). tures, which are formed by green and bluegreen A collection made by E. Isaac on the reef algal films that trap and bind sediment in the flats in Kenya produced five species of Neo- lower areas of the intertidal zone, or in shallow goniolithon, one species of Porolithon, two submerged shoal areas (Logan and others, species of Mesophyllum, and one species each 1964). Bosellini and Ginsburg (1971) called of Hydrolithon, Tenarea, Heteroderma, Melo- these crustose coralline algal deposits "rhodo- besia, and Archeolithothamnium (Adey, unpub.). lites" but recently proposed the term "rho- In a quantitative study of depth distribution doid" (Bosellini and Ginsburg, 1973), since of crustose corallines in the Hawaiian Chain, "rhodolite" refers to a variety of garnet Lithophyllum, Neogoniolithon, and Porolithon (Binda, 1973). Etymologically, the earlier formed about 85 percent of the cover down term "rhodolith" (Barnes and others, 1970; to 10 m, whereas Lithothamnium occurred in Barnes and others, 1971) may be more suitable only trace quantities. However, Lithothamnium in this context, and consequently it is preferred and Hydrolithon species become the dominants in this discussion. The relation between rhodo- at depths greater than 40 m, but primarily as liths and environment is discussed further nodule formers (Adey and W. T. Boykins, below. in prep.). Owing to earlier "umbrella" terminology, It becomes apparent, therefore, that in carbonate sedimentologists tend to equate the tropical, shallow-water reef environments of term Lithothamnion with crustose coralline the Atlantic and Indo-Pacific, anywhere from algae when identifying component grains in five to fifteen species belonging to ten genera sediment samples. The following list of exam- may commonly occur; however, the total ples illustrates this ambiguity: species list may be three to five times that number. The dominant components, however, No attempt was made to separate these various belong to the genera Neogoniolithon, Porolithon, cerioid forms, and the term Lithothamnion is here used to include, Lithothamnion, Lithophyllum, and Lithophyllum (see Appendix1) and the Goniophyllum et cetera (Illing, 1954, p. 20); Melobesioideae are weakly represented by Mesophyllum and Archeolithothamnium, with The most abundant type [of coralline algae] in- Lithothamnium either absent or relatively un- cludes the encrusting Lithothamnion and related genera, and branching forms like Goniolithon important in cryptic situations. (Ginsburg, 1956, p. 2424); The common use of Lithothamnion to denote . . . Lithothamnion and other calcareous red algae all crustose corallines, particularly in tropical (Emery, 1962, p. B20). areas, has also resulted in the misnomer, "Lithothamnion balls." This term is commonly Because Lithothamnium is generally a deeper applied to spheroidal agglomerations of en- water or arctic water genus, it is not illogical to crusting components that consist predomi- assume that Lithothamnium species are not nantly of crustose coralline algae; when broken, major contributors to sediments in modern these balls exhibit irregular concentric layer- shallow-water tropical areas, where the above ing. Although the coralline algal component investigators worked. has been identified as Lithothamnium in some studies (Ludwick and Walton, 1957; Bosellini PROBLEMS IN ENVIRONMENTAL and Ginsburg, 1971), in most cases, identifica- STUDIES tion has not been made (Stetson, 1953; Parker The spectacular Pacific algal ridges are well documented in the geological literature (for 'Appendix (NAPS no. 02013) may be obtained by example, see Tracey and others, 1948; and writing to CCM Information Corp.-NAPS, 909 Third Ladd and others, 1950), but the "algal ridge" Ave., New York, New York 10022, enclosing $5 for associated with coral reefs was considered to be photocopies, or $2 for microfiche. Make checks payable to lacking in the Atlantic-Caribbean. However, NAPS. studies from the Atlantic-Caribbean, particu-
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larly within the last decade, have reported arcticum characterized the vegetation of a large small structures variously referred to as: tract at Uddebay in the Kara Sea. ... It is the "microatolls" (Yucatan, Boyd and others, Corallinaceae that stamp the vegetation with its 1963; Panama, P. W. Glynn, 1971, personal general character. commun.); "cup reefs" (Bermuda, Ginsburg Furthermore, Svendsen (1959) reported that and others, 1971); "formations de vermits et around Spitzbergen: d'algues calcaires" (Brazil, Kempf anc. La- borel, 1968); "reefs of Lithophyllum antil- At depths greater thin 20 m various Rhod- larum and Lithophyllum daedalum" (Pjerto ophyceae, in particular Lithothamnion, were usually Rico, Howe, 1912); and "boilers," personal the most important algae (p. 23). observations, St. Croix. Further, a "Recent According to Jonsson Lithothamnion may be study of an offshore barrier-like reef on the abundant at 88 m depth. At East Greenland Atlantic side of Panama conclusively confirms (Scoresby-Sound) Lund records the presence of the existence of an algal ridge formation in Lithoderma, Cruoria and Lithothamnion at a depth this part of the Caribbean Sea" (Glynn, 1971, of 120 m (p. 26). p. 18-19). Our recent observations in the Caribbean region indicate that the crustose The abundance of crustose corallines in non- corallines may be significant, if not dominant tropical waters is also described in a study in components in many shallow-water reef areas. the western North Atlantic subarctic (Adey, It is also interesting to note that Porolithon 1966b, p. 9-10): pachydermum, which is a major shallow-wc.ter While crustose corallines are abundant nearly species on exposed reefs, is very similar to ;.nd everywhere on shallow rocky bottoms in the Gulf perhaps only a variety of Porolithon onkodes, of Maine, and expanses of coralline ledge or boulder the major Pacific ridge-former. largely free of other algae and small bands of maerl Smaller but similar and well-known struc- do occur, especially in the large Maine bays, they tures in the Mediterranean, composed mainly are frequently covered, especially in exposed localities, with heavy growths of filamentous, leafy of Lithophyllum tortuosum and Neogoniolithon and fleshy algae. In the areas under discussion, notarisii, have generally been referred to as and especially in sou-hern Nova Scotia, Newfound- "trottoir à Tenarea." However, the generic land, sout-iern Labrador and the northern Gulf designation Tenarea was improperly applied to of St. Lawrence, the overlying algae are somewhat L. tortuosum and the more recent terminology reduced in abundance, and from about 1-25 meters is "corniche of Lithophyllum tortuosum" (Pérès, a conspicuous coralline coating often 2-3 cm. thick 1967). and ranging up to about 10 cm. thick is developed. In addition to the abundant epifauna of mollusks The general conspicuous development of and echinoderms, these microbiostromes generally crustose corallines in warm, turbulent, shallow contain a strong infauna of boring pelecypods and waters has led to the mistaken impression that ophiurans. In semi-exposed localities, such as bays crustose corallines are uniquely characteristic and fjords, the thick, Lithothamnium plants that of such environmental conditions. However, are broken free of the ledge boulder bottom in crustose coralline algae thrive in polar as well shallow water continue to grow as they move as tropical conditions, and they commonly downslope or collect in the crevices. In some cases form the dominant component of benthic a narrow but thick band of maerl develops below the ledge-boalder-cobble bottom. communities from the intertidal zone down to the lower limit of the photic zone. For ex- Also, in boreal-subarctic Norway, luxuriant ample, Kjellman (1883, p. 11-12) found: growths form extensive ridges:
Very extensive parts of the sublittoral zone of . . . widely extended banks—even as far as about the Arctic Sea are occupied by Corallinaceae. 3 km. in length, composed of millions of individuals . . . Lithothamnium glaciale is abundant at several up to four or five specie.!, not only of smaller forms, places on the coast of Spitzbergen; at the mouth of but the large ones up to nearly 2 feet in diameter Musselbay, it covered the bottom to the extent of (Foslie, 1894, p. 39). 4-5 English square miles, in the form of balls that had a diameter of 15-20 cm2. Even on the west coast of Novaya Zemlya, I have found a vegetation Although these banks occur in water as shallow of Lithothamnium glaciale, rich in individuals, as 1 to 2 m, they are generally found, especially growing in regions of considerable extent. ... In in the north, at depths of 20 to 30 m. In some the same manner, a Coralline, (Lithophyllum) areas, similar postglacial deposits of crustose
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corallines are subaerially exposed and are tropical waters. In the Mediterranean, active quarried for road material; at Bodo Norway maerl deposits are known to depths of 60 to 65 (lat 67.5 N.), Adey has seen a cut face exceed- m in the western basin, and down to 160 to ing 3 m in thickness. 180 m in the clearer, warmer eastern basin. On On the boreal-temperate European Atlantic hard substrate, crustose corallines of the genera Coast, the English, French, and Spanish rias Lithophyllum, Neogoniolithon, and Mesophyllum typically have extensive deposits of maerl, are important elements of the "coralligenous loose bottoms of living and dead Phymatolithon biocoenosis" occurring to depths of 120 to calcareum and Lithothamnium coralloides, gen- 130 m in the eastern basin (Pérès, 1967). Living erally from 5 to 40 mm in diameter (Vanney, crustose corallines have been observed from a 1965; Guilcher and Pruleau, 1963; Berthois submarine as major elements on steep reef and Guilcher, 1959; Koldijk, 1968; and Adey walls at 150 to 200 m off British Honduras (J. and McKibbin, 1970). Earlier knowledge of C. Lang, 1971, personal commun.), and at these deposits was documented: depths down to 200 m in the Tongue of the Ocean, Bahamas (J. W. Porter, 1972, personal La découverte du Maerl est Très ancienne . . . commun.). d'après Ray en 1724 il était déjà récolte à Falmouth Haven (English Channel) pour le chaulage des Rhodoliths are a characteristic element of the terres de Cornouailles" (Jacquotte, 1962). sea floor at depths of about 50 to 150 m on Although maerl deposits may extend to 20-25 many oceanic offshore banks and continental meters, they are generally best developed at or insular margins: Challenger Bank, southeast 3-10 m depth. Similar beds have been described of Bermuda (Thomson, 1877, p. 360); the for the Mediterranean, where the Lithophyllum Bermuda slope (50 m, B. C. Coull, 1970, per- species begin to play an important role sonal commun.); slope of Kure Atoll (40 m, (Jacquotte, I.e., 1962). Ladd, 1968, personal commun.), and Nero It is also readily apparent from the following Bank (200 to 300 m; Ladd, 1968, personal observations that these occurrences are not commun.), Hawaiian Chain (55 to 92 m, Adey, only a North Atlantic phenomenon: personal observation) (see also Table 1 and Bosellini and Ginsburg, 1971, p. 670). Al- One of the most striking observations concerning though rhodoliths frequently have living crusts the coralline algae on Amchitka (Aleutian Is.) is on their surfaces, radiocarbon dating of crustose their very high abundance on the bottom. In coralline material collected from depths greater numerous SCUBA dives from the surface to 30 than 50 m indicates that, at least at their lower meters, we have observed very few instances of limits of occurrence, most of the skeletal suitable rock substrate that was not occupied by structure is relict (Table 1). However, in view corallines. Underwater photographs indicate that of the data presented by McMaster and crustose corallines frequently cover 50-70% and sometimes nearly 100% of the bottom. (Norris Conover (1966, and 1971, personal commun.), and Lebednik, 1970, p. 4). it would appear that rhodoliths can actively form at least down to depths of 60 to 70 m. The single most abundant coralline species on Because of their likely slow rates of growth Amchitka is Clathromorphum loculosum which is (see Adey, 1970b), especially in deep water, a apparently confined to the Bering Sea islands. This continuously growing rhodolith of 20 to 30 cm species forms massive incrustations up to 30 cm. in thickness on the rocky ledge bottoms. (Norris and diameter would be expected to give core ages Lebednik, 1970, p. 6). of at least 500 to 800 yrs. Considering likely burial, exhumation, and occasional damage by In the Antarctic: browsing animals, actual ages could be expected to be much higher. Careful radiocarbon dating "Ces algues (Mélobésiées) sont souvent si abon- of rhodolith layers, surface to core, could give dantes un peu au-dessous de la limite de la basse valuable data on the origin and development of mer qu'elles forment une ceinture continue sur les these structures. rochers; elles recouvrent tous les galets, et on rencontre habituellement plusiers espèces sur les It is evident from the preceding observations mêms caillous (Lemoine, 1913). and from the wide depth range of crustose corallines—down to about 200 m (Cloud, In addition to their importance in deep, 1952)—that without some knowledge of the photic arctic waters, crustose corallines can genera and their environmental limitations, also be a major constituent of the epibenthic paleoenvironments cannot be interpreted sim- community in relatively deep temperate to ply from the occurrence of crustose coralline
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Water depth Locality Material in meters Age
Southern Coralline algae California* encrusting pebbles 108 to 118 24,500 ±1,600 (Emery, 1958) (142 to 249 cm below sed. surface) Broken and reworked coralline algal material 116 17,000 ± 1,400 (0 to 51 cm below sed. surface) Broken and reworked coralline algal material 108 18,600 ± 1,200 (0 to 158 cm below sed. surface) Coralline algae encrusting pebbles :.02 to 105 20,000 ± 1,000 (147 to 325 cm below sed. surface)
Paria—Trinidad Fragments of Shelf* coralline algae 186 14,220 ± 350 (Koldewijn, 1958) (40 cm below sed. surface) Fragments of coralline algae 156 13,800 ± 330 (94 cm below sed. surface) Coralline algal limestone L 9 to 128 13,720 ± 330 Fragments of coralline algae and corals 86 9,930 ± 240 (155 to 180 cm below sed. surface) Western Guiana Calcareous masses, Shelft including coralline algae 103 12,165 ± 350 (Nota, 1958, and personal commun., 1971) Calcareous masses, including coralline algae 128 11,560 ± 240 Canary Islands* Crust of coralline (McMaster and algal ball 63 to 66 400 ± 40 Conover, 1966) Core of cora'line algal ball 63 to 66 1,500 ± 100
North Carolina? Coralline algal (Menzies and others, 1966) components from algal balls 90 19,200 ± 650 (Macintyre and Coralline algal Milliman, 1970) components from algal limestone 99 to 108 12,270 ± 190 Coralline algal components from partly recrystallized algal limestone 54 to 94 26,250 ± 900 800
East coast of Coralline algal Florida? components from (Macintvre and algal limestone 74 to 81 11,170 ± 160 Milliman, 1970) South African Coralline algal balls 115 13,670 ± 120 ShelfS (Siesser, 1972) Coralline algal balls 120 12,990 ± 100 * Core samples, t Grab or dredge samples. 5 Trawl or dredge samples.
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algae. Even the suggestion that large quantities the outer United States Atlantic shelf: "Oo- of algal limestone indicate "warm-water for- lites, beachrock, and coralline algae are strand- mation" (Cloud, 1952, p. 2134) is not a valid line deposits that form under warm climatic inference. After completing field work in conditions" (Friedman and Sanders, 1970, p. Newfoundland, and more recently in the 2457). The oolites and beachrock are correctly Bahamas and Virgin Islands, Adey is of the interpreted as near strandline deposits, but it opinion that crustose corallines generally have is obvious from the habitat of modern species a more extensive bottom coverage and are more that crustose coralline algal limestone cannot important in determining the nature of bottom be used to infer tropical shallow-water condi- fauna in Newfoundland than in the other two tions. areas. Unfortunately, a number of errors have been CRUSTOSE CORALLINE TAXONOMY made in paleoenvironmental interpretations based on coralline algal distribution. For ex- Literature ample, it was assumed that prominences in the Since 1800, approximately 220 scientific northeastern Gulf of Mexico formed under papers have appeared which either specifically shallow-water conditions because "Calcareous treat Holocene crustose corallines or add signifi- algae (genus Lithothamnion), the chief con- cantly to our knowledge of the group (Fig. 1). stituent of the reef rock and surrounding sedi- Yet, no really comprehensive work has ever ment, are not found living on or near the been published by the few coralline specialists pinnacles. This genus lives in shallow water and summing our knowledge to date. M. Foslie, a its presence in the pinnacles today indicates Norwegian who amassed collections from the that they were formed originally in shallow coasts of virtually the entire world ocean (Adey water" (Ludwick and Walton, 1957, p. 2100). and Lebednik, 1967), and produced about 75 These topographic features may very well have percent of the papers in the 1890-1910 interval, been formed in pre-existing shallow-water intended a monograph, but only a partly com- conditions, but their association with crustose pleted paper, largely a collection of photo- coralline algae does not necessarily support this graphs, was published posthumously in 1929. hypothesis. Also questionable is the assumption During the interval 1910-1940, Madame that the probable position of sea level at the Lemoine produced 75 percent of the papers, time of crustose coralline algae formation is primarily regional studies; whereas in the limited to within 30 m above the depth of its 1940s, Svante Suneson was the only worker of occurrence (Hopkins, 1959, p. 1525). It has importance. But after the 1920s, even the been suggested that "coralline algae and specialists tended to ignore the accomplish- hermatypic corals can be used as sea-level ments of the earlier workers and many of the indicators, but only with care, because certain nonspecialists retreated to a pre-1900 level of species can live in depths greater than 20 m" knowledge, rather than trying to sort and (Milliman and Emery, 1968, p. 1123); the build on the basis of what had been accom- caution expressed here is an understatement plished. Fifteen of the genera (or their basic with regard to the crustose corallines, which concepts; for example, Lithothamnium, Litho- can grow in depths up to ten times greater than is cited. Furthermore, it has even been suggested that crustose coralline algae are indicative of shallow- and warm-water conditions; crustose coralline algal limestone dredged from the North Carolina shelf edge by Menzies and others (1966), for example, was described as "submerged Quaternary 'tropical' strandline carbonates" (Sanders and Friedman, 1969, p. 1793). In a subsequent discussion of climatic conditions during pre-existing sea levels, warm 85 95 1905 15 25 35 45 55 65 75 Figure 1. Approximate number of papers published conditions coinciding with low sea levels were per decade (for example, 1910-1919) specifically or interpreted partly on the basis of the occur- significantly treating Holocene (source, Adey's lit. file) rence of crustose coralline algal limestone on and fossil (source, Johnson, 1961) crustose corallines.
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phyllum, and Melobesid) were established iro n 1890 to 1923 (Fig. 2). From that point until the late 1950s, interest in the group was mini- mal, the number of published papers greatly decreased; and, with few exceptions, what was published tended to be repetitive or contain very basic descriptions of species. In contrast, the interest and productivity of fossil coralline workers show a largely con- sistent increase after 1890. The first modern genus was solidly established (Archeolithc- i 1875 85 95 190!)"¡5 ¿5 35 45 55 65 75 thamnium) and the most basic reproductive Figure 2. Number of presently accepted generic difference between the Lithothamnium grouo concepts established per decadi:. and the Lithophyllum group was developed by and do not consider the inherent, environ- a paleobotanist (Rothpletz, 1891). His phycolo- mentally induced, variation present in crustose gist contemporaries (primarily Foslie) devel- corallines. Cytological, anatomical, and popula- oped the modern concepts of the group from tion approaches, along with studies of type there. Several treatments emphasizing crustose collections, have begun to break down this dif- coralline fossils have been written by paleo- ficulty. Wherever possible, if Holocene collec- botanists (Conti, 1950; Johnson, 1961). How- tions are described in detail, as discussed below, ever, while the latter book (which was virtually on the basis of several plants and with reference a state-of-the-art treatment), has been generally to the now generally available type materials available to geologists and oceanographers, it for many species (see Adey. 1970a), the specific did not prevent the development of many of identification problem should in most cases the cited misunderstandings. Recently, Wray gradually disappear. It will perhaps be some (1971) presented an excellent summary of time before the applicability of "new" tech- "Algae in Reefs Through Time." niques now applied to Holocene plants can be fully tested with fossil material. For the most part, the basic generic-level crustose coralline taxonomy established at the Members of all three crustose coralline sub- turn of the century has required little revision. families date from mid- :o upper Mesozoic, The more intensive cytologic-anatomic studies and perhaps they are not even directly related, of the past decade have in many cases firmly having developed from separate ancestors, pos- established earlier generic groupings, and a sibly different genera of Squamariaceae with as considerable amount of new information on many as four or five phylogenetic lines in- intergeneric relations, as well as a few new volved (Fig. 3) (see Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 CRUSTOSE CORALLINE ALGAE 891 • Known as fossils,range • not known as fossils, though perhaps identified asLithofhomniumfilc. age hypothetical. S RECENT 111! s " §'. € * * PLEISTOCENE J: •S • • PLIOCENE s: £ MIOCENE sS' I/ OLIGOCENE EOCENE PALEOCENE CRETACEOUS •..I f$ JURASSIC Figure 3. Hypothetical evolutionary history of provided in Johnson, 1961, Adey, 1970a, and Lemoine, crustose coralline algae. Adapted from information 1971. The basic phylogenetic differentiation in asexual conceptacles, and is aimed toward crustose corallines is the development of thick- generic breakdown wherever possible with walled, asexual sporangial caps in the Melo- minimum preparation. A 30-50X dissecting besioideae (that is, multipored asexual con- microscope is critical for this work (up to 80X ceptacles). This differentiation has perhaps led is desirable for presectioning procedure). to some of the hesitancy of nonspecialists to work with corallines, as the statement that ECOLOGY OF CRUSTOSE asexual conceptacles or microtome sections are CORALLINES required before any generic identification can Because they can be treated in terms of be attempted, is common in the literature. This surface area, most crustose corallines are well may be true in some cases, and conceptacles suited for quantitative ecological studies. Once and sectioning is always desirable, but fre- the obstacles arising from taxonomic problems quently not necessary. The working key generally are overcome, it seems likely that (Table 4) is based on the possible absence of the group will be included more often in TABLE 2. SUPRAGENERIC CLASSIFICATION ecological studies, or may even become "popu- OF THE RECENT CRUSTOSE lar subjects." CORALLINE ALGAE Light is the primary factor controlling the depth distribution of crustose corallines, and Subfamily Lithophylloideae Setchell 1943 most species in arctic to temperate waters are Tribe Lithophylleae (Setchell) Mason 1953 Lithophyllum, Tenarea known to have limited depth ranges in this Subfamily Mastophoroideae (Svedelius) Setchell 1943 respect (Adey, 1971, 1966a; Adey and Adey, Tribe Pseudolithophylleae Adey et Johansen 1972 1973). Limitations relative to light conditions (Pseudolithophylleae) are even more marked in the tropics (Adey, Pseudolithophyllum, Heteroderma, Choreonema (Porolitheae) in prep.). On the generic level, depth zonation Hydrolithon, Fosliella, Neogoniolithon, Porolithon among the crustose corallines cannot be as Tribe Mastophoreae Svedelius 1911 sharply delineated, although most genera have Metamastophora, Lithoporella more or less characteristic ranges of occurrence Subfamily Melobesioideae (J. Aresch.) Mason 1953 Tribe Melobesieae J. Aresch. 1852 (Table 5), which again are more distinct in the Melobesta, Archeolithothamnium, Lithothamnium, tropics than to the north. Up to now, studies Clathromorphum, Neopolyporolithon, Mesophyllum containing data on depth distribution have Tribe Phymatolitheae Adey et Johansen 1972 considered mainly the depth of occurrence of Phymatolithon, Leptophytum, Kvaleya the crustose corallines while overlooking light Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 892 ADEY AND MACINTYRE TABLE 3. "NATURAL" KEY TO THE GENERA OF RECENT CRUSTOSE CORALLINE ALGAE 1. Asexual sporangia without caps, that is, conccptacles single-pored (Figs. 4 through 6) 2. Secondary pits present in perithallium (Figs. 12, 13) Li thophy Uoideae 3. Palisade, single-layered hypothallium (Fig. 12) T.marea Bory 1832 3. Non-palisade, single-layered (Fig. 13) or multilayered coaxial hypothallium Lithophyllum Philippi 1837 . Secondary pits absent, fusions present (Figs. 15 through 18) M astophoroideae 4. Heterocysts present (Figs. 15 through 18) (Porolitheae) 5. Hypothallium single layered (Figs. 12 through 14) 6. Perithallium well-developed and irregular due to wide variation in cell size Hydrolithon Foslie 1909 6. Perithallium weak, except around conceptacles Fosliella Howe 1920 5. Hypothallium multilayered (Figs. 19 through 25) 7. Heterocysts vertical rows or single pigs. 17, 18) Neogoniolithon Setchell & Mason 1943 7. Heterocysts horizontal rows (Fig. 15) P-.rolithon Foslie 1909 4. Heterocysts absent (Pseudolithophylleae and Mastophoreae) 8. Free-living plants 9. Crustose plants 10. Perithallium well-developed Ps;udolithophyllum Lemoine 1913 10. Perithallium weakly developed or absent in vegetative plant 11. Intensive overgrowing, large cells (>10 to 15/J diam.) Luhoporella Foslie 1909 11. Overgrowing weak, small cells Heteroderma* Foslie 1909 9. Leafy, upright plants, palisade hypothallium Metamastophora Setchell 6c Mason 1943 8. Parasitic plants Choreonema Schmitz 1889 * Note: With further study, it may be determined that all Heteroderma species are potentially able to have hetero- cysts (trichocytes). In this case, Fosliella would no longer be used. 1. Asexual sporangia with caps, that is, asexual conceptacles multipored (Figs. 7 through 11) Melobesioideae 12. Large-celled meristem, growth by meristem elongation (Figs. 27, 29) Mslobesieae 13. Multilayered hypothallium 14. Lithothamnium cover cells (Fig. 27) 15. Asexual sporangia in broad sori (Fig. 26) At cheolithothamnium' Rothpietz 1891 15. Asexual sporangia in conceptacles Lithothamnium Philippi 1835 14. non-Lithothamnium cover cells 16. Coaxial hypothallium (Figs. 19, 20) M'tsophyllum Lemoine 1923 16. Parallel, noncoaxial hypothallium 17. Epithallium well-developed, photosynthetic (Fig. 29) (Adey, 1965b) Cluhromorphüm Foslie 1898 17. Epithallium weak, nonphotosynthetic Ntopolyporolithon Adey & Johansen 1972 13. Single-layered hypothallium Mdobesia Lamouroux 1812 12. Small-celled meristem, growth by progressive elongation (Fig. 28) P.r.ymatolitheae 18. Conceptacle primordia deeply sunken (Fig. 7) Phymalolithon Foslie 1898 18. Conceptacle primordia shallow 19. Free-living Leptophytum Adey 1966 19. Parasitic Kialeya Adey & Sperapani 1971 t Note: Structures similar to secondary pits (as well as fusions) have been reported for Archeolilhothamnium (Ca- bioch, 1970). conditions at a given depth. The light factor some genera are virtually restricted to tropical- may be even more critical than previously subtropical waters (Porolithon, Neogoniolithon, indicated, and future work based on this con- Hydrolithon, Lithopore.'la and Archeolithotham- trolling parameter may indeed show zonations niuiri). Only two genera, Clathromorphum and to be considerably more distinct relative to the parasite Kvaleya, ai e restricted to the arctic light conditions. or subarctic. Mesophyllum and Pseudolitho- The influence of temperature on the ecology phyllum are primarily antarctic and Litho- of crustose corallines is certainly evident in that thamnium arctic in occurrence. However, all Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 CRUSTOSE CORALLINE ALGAE 893 Figure 5 lOOjU Figures 4, 5, 6. Development of asexual conceptacles stage, 6. mature conceptacle. spi-sporangia initial; in Tenarea sp. (Adey, 1965a); 4. primordial, 5. mid- bsp-bispores. Figure 7 5QM Figures 7, 8,9. Development of asexual conceptacles cap; spi-sporangia initial; spc-sporangial cap; tsp- in Phymatolithon calcareum (Adey and McKibbin, 1970) ; tetraspores. 7. primordial, 8. mid-stage, 9. mature, cc-conceptacle three of the latter genera do extend to warmer level, very sharp cut-off temperatures have waters, although for the most part they occur been recorded (Aden, 1971, and in prep.), so in deep water or cryptic situations (see Ap- that temperature controls are thought to be pendix1). The very generalized observation of more limiting than previously contemplated. Melobesioideae in colder waters and Masto- However, additional studies obviously are re- phoroideae (and to a lesser extent Litho- quired to determine the mechanisms involved. phylloideae) in warmer waters has been known Another important factor controlling crus- for decades (see Johnson, 1961). On the specific tose coralline occurrence is that of salinity Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 894 ADEY AND MACINTYRE Figure 10 50// Figures 10, 11. Development of asexual conccptacles y in Lithothamnium coralloides (Adey and McKibbin, 1970); 10. mid-stage, 11. mature, cc-conceptacle cap; spc-sporangial cap; tsp-tetraspores. levels, for very few species tolerate low salini- comparison to theii: northern counterparts. ties. While the widespread intertidal and orack- Quantitative data on this aspect of crustose ish species Phymatolithon lenormandii may tol- coralline ecology, however, are still lacking. erate continued levels of 10 to 15%, and Among the prime factors controlling distri- Phymatolithon laevigatum and P. polymorphism bution of crustose corallines are substrate and can withstand continued levels of about 20gc, wave action. In terms of bottom types, the most other species require at least coastal crustose corallines car. be placed in two major salinities greater than 25 %o- Perhaps there are groupings: (1) those encrusting a fixed sub- finer tolerances between 25 %o and 35 %c, but strate, animal or plant, noncarbonate or car- these do not appear to be marked. bonate rock, and (2) those encrusting an The effects of the grazing activities of unstable organic or mineral substrate, or animals on crustose corallines are little under- actually forming a major part of the sediment. stood. Although intensive grazing by some The two types intergtade depending upon the larger organisms may actually kill or limit environment. Relative to the crustose coral- crustose corallines, it seems more likely that lines in northern waters, a substrate that most grazing is beneficial in that competitors, remains essentially fixed for 10 to 50 years or especially in the form of fleshy algae, are re- more would be stable; less than one year would moved or greatly limited in this way. Maine be unstable. Perhaps in shallow water in the lobstermen have observed, for example, several- tropics, shorter periods are involved. year cycles in kelp beds where heavy kelp The distributions of the fixed substrate type growth and few sea urchins occur some years, in arctic-boreal waters have been studied whereas coralline bottoms are virtually bare quantitatively by Adey (1964, 1966a, 1968, and urchins abundant in other years. An 1970c) who showed that most species of crus- abundance of echinoderm and mollusc grazers tose corallines have definite substrate size are certainly characteristic of the rich coralline (Fig. 30), geographic and depth limitations. bottoms of Newfoundland. In some cases, Quantitative studies Li progress indicate that grazers may even show a symbiotic relation similar though more restrictive distribution with coralline crusts (Adey, in prep.). patterns and controls are present in tropical Space competition, particularly with sclerac- waters (Adey and W. T. Boy kins, in prep.). tinian corals, millepores, and sponges, is The second type, crustose corallines occupy- especially important to coralline abundance in ing or forming an unstable substrate (free tropical waters. Little information is available corallines, maerl, rhodoliths), have been of on the factors involved, but growth rates obvi- considerable interest to geologists. The very ously are critical to survival under strong com- wide geographic and depth range of their oc- petition as probably indicated by the relatively currence was briefly described above. While it faster growth of tropical crustose corallines in would appear that the existence of many Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 CRUSTOSE CORALLINE ALGAE 895 100JU Figure 24 Figure 12. Palisade hypothallium in Tenarea sp. (Adey, 1965a). hc-heterocyst, trichocyte; fs-fusions. (Adey, 1965a). ep-epithallium; pr-perithallium; sc- Figure 18. Vertical heterocyst chain in Neogonioli- secondary pits; hy-hypothallium. thon sp (Adey, 1965a). hc-heterocyst, trichocyte. Figure 13. Isodiametric, single-layered hypothallium Figures 19, 20. Coaxial hypothallium in Mesophyl- in Lithophyllum orbiculatum (Adey, 1965a). ep-epithal- lum lichenoides (Suneson, 1937). ep-epithallium; hy- lium; sc-secondary pits; hy-hypothallium. hypothallium; pr-perithallium. Figure 14. Trichocytes in Fosliella sp. (Adey, Figures 21-25. Parallel, non-coaxial hypothallia 1965a). hy-hypothallium. in Phymatolithon and Lithothamnium spp. (Kylin, 1956). Figures 15, 16. Horizontal heterocyst field in pr-perithallium; hy-hypothallium. Porolithon sp. 15. at surface, 16. buried (Adey, 1965a). Figure 26. Sporangial sori in Archeolithothamnium hc-heterocyst, trichocyte; fs-fusions. (after spore release), ep-epithallium; so-sori. Figure 17. Single heterocyst in Neogoniolithon sp. rhodolith substrates depends upon a supply of change in the size of the encrusted ball and material fragmented from an encrusted stable not necessarily a change otherwise in environ- substrate, once developed, a rhodolith bottom, ment. at least under some conditions, can probably Very thin and rapidly growing genera, such support itself by fragmentation and growth. as Fosliella, commonly develop on bare pebbles This aspect of rhodolith development is virtu- newly made available for colonization, and ally unstudied (Adey and McKibbin, 1970). unless the pebble is very unstable, these plants Since ability of a coralline species to survive are soon covered by other corallines, algae, or on an unstable substrate varies widely from animals. In general, strictly crustose types are species to species (Fig. 30), a change in the not shallow-water rhodolith formers, although dominant species of crustose coralline within a they may grow apical "leafy" crusts (as is rhodolith's internal structure may reflect a characteristic of Mesophyllum and Neogonio- Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 \0/j Figure 27. Upper perithallium and epithallium in Figure 28. Upper perithallium and epithallium in Figure 29. Upper perithallium and epithallium in Lithothamnium coralloides (Adey and McKibbin, 1970). Phymatolithon calcareum (Adey and McKibbin, 1970). Neopolyporolithon reclinatum (Adey and Johansen, ep-epithallium ; mr-meristem ; pr-perithallium. ep-epithallium; mr-meristem; pr-perithallium. 1971). ep-epithallium; mr-meristem; pr-perithallium. Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 TABLE 4. WORKING KEY TO THE GENERA OF RECENT CRUSTOSE CORALLINE ALGAE D—dissecting microscope required M—microtome sections required Dl. Multipored asexual conceptacles present D2. Plants small, white—parasitic on other crustose corallines Kvaleya D2. Free-living D3. Plants primarily a single-layered hypothallium (perith. absent except around conceptacles) Melobesia D3. Plants with well-developed perithallium D4. Hypothallium coaxial on radial fracture Mesophyllum D4. Hypothallium noncoaxial D5. Large sunken meristem obvious on vertical fracture D6. Epithallium 4 or more cells and strongly pigmented Clathromorphum D6. Epithallium 2 or 3 cells, nonpigmented or weakly pigmented Neopo lyporo lit ho n D5. Sunken meristem not obvious Ml. Lithothamnium cover cells, large meristem Lithothamnium Ml. Noii'Lit/iothamnium cover cells—small-celled meristem M2. Pore cells present, conceptacles strongly raised Leptophytum M2. Pore cells absent, conceptacles sunken or weakly raised Phymatolithon Dl. Sporangia in sori, sporangial caps visible Archeolithothamnium Dl. No multipored asexual conceptacles or sori D7. Parasitic on other corallines, only conceptacles visible on surface D8. On articulates Choreonema D8. On crustose corallines Kvaleya D7. Free living D9. Upright, leafy, flexible Metamastophora D9. Crustose or if leafy, nonflexible D10. Individual crusts extremely thin (if thick, by overlapping), primarily hypothallium Dll. Large cells ( >10 to 15/i diam) Lithoporella Dll. Smaller cells D14. Palisade hypothallial cells on vertical fracture Tenarea D14. Isodiametric hypothallial cells D15. Heterocysts or trichocytes Fosliella D15. Heterocysts lacking Melobesia D10. Thicker crusts, developing perithallium Heteroderma D16. Heterocysts present D17. In fields D17. Single Porolithon D18. Hypothallium obviously coaxial or multilayered on fractured section D18. Not coaxial or if multilayered thin Neogoniolithon D19. Perithallium granular in appearance D19. Nongranular Hydrolithon D16. Heterocysts absent (may have to be verified with paraffin sections) Neogo nio lit h on D20. Surface distinctly glossy and generally deep brownish-red, or buried sporangial sori obvious on vertical fracture Archeolithothamnium D20. Surface dull, buried sori absent D21. Hypothallium coaxial on radial fracture Mesophyllum D21. Hypothallium noncoaxial D22. Large sunken meristem obvious on vertical fracture D23. Epithallium 4 or more cells and strongly pigmented Clathromorphum D23. Epithallium 0 to 3 cells, nonpgimented or weakly pigmented D24. Large diam cells ( > lO/i diam) Neopolyporolithon D22 and D24. Cells relatively small Ml. Secondary pits M2. Palisade hypothallium Tenarea M2. Nonpalisade hypothallium Lithophyllum Ml. No secondary pits (fusions) M3. Lithothamnium cover cells Lithothamnium (Archeolithothamnium) M3. non-Lithothamnium cover cells Phymatolithon Leptophytum (Conceptacles necessary) A series of phytogeographic maps indicating the geographic distribution of most of the Holocene crustose coralline genera has been published (Adey, 1970a). These were included as Figures 32 through 44 in the manuscript of this paper. However, it was not possible to include them in the final draft. They are being deposited with NAPS as a retrievable appendix to this paper. See footnote 1, p. 885. Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 898 ADEY AND MACINTYRE TABLE 5. GENERALIZED LIGHT REQUIREMENTS FOR SOME CRUSTOSE CORALLINE GENERA lithon, and some Phymatolithon species). Rather, is current or wave action. Excessively strong the branching species generally are the domi- water motion prevents the relatively light and nant rhodolith formers, and among them fragile rhodoliths from forming, whereas weak bithothamnium is the most predominant, al- wave or current action leads either to their though Neogoniolithon, Archeolithothamnium, stabilization through growth and coalescence Lithophyllum, and Phymatolithon also have of crusts or to burial by fine sediment that branching species that are involved in the eventually kills the crustcse corallines. The construction of rhodoliths. In deep tropical small percentage of living plants on the surface waters, crustose types are perhaps more im- of deeper rhodoliths indicates a marginal exis- portant in rhodolith formation, but even many tence for the crustose: corallines and probably of these are probably Lithothamnium or Archeo- an extremely slow rate of rhodolith growth. lithothamnium "branching species" that have A theoretical diagram of the occurrence of highly reduced branching in the deep environ- crusts and rhodoliths as a function of wave ment. The deep (greater than 50 m) tropical action and turbidity is given in Figure 31. The rhodolith nodules especially need detailed complex interaction of controlling factors of study. rhodolith formation must be taken into ac- Although a complex set of physical, chemi- count in paleoecological interpretations. For cal, and biotic factors probably controls the example, in more turbid northern waters, distribution of rhodoliths, the primary factor rhodoliths are found only in relatively shallow Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 SHALLOW (0-3M.) DEEP (30-40M.) JmmmMmm %Morbicu/atum 1000 1000 SPECIMEN WEIGHT (GM.) SPECIMEN WEIGHT (GM.) frequently occasionally occasionally fixed overturning overturning overturning Figure 30. Occurrence of major crustose coralline ern, and eastern Iceland (after Adey, 1971). species on pebble-cobble substrate off western, north- Limit FJORD, BAY OR LAGOON photic zone ENTRANCE INNER BAY (-i-corallines) Turbid •—(Gulf of Maine, 20 British Isles) Clear coastal (Newfoundland, "4° NW Norway) Clear tropical -60 -80 •100 120 •140 160 DECREASING ENERGY ON BOTTOM Figure 31. Idealized diagram of the occurrence of any depth to about 200 m in clear waters where a steep various coralline morphological-habitat types as a enough slope exists—deep encrusting types are char- function of wave exposure, depth, and turbidity (cur- acteristic on steep "reef" faces), rent effects not considered; ledge coatings can occur at Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 900 ADEY AND MACINTYRE and protected waters (the bays, fjords, and TABLE 6. SPECIFIC EXAMPLES OF RHODO- rias of Maine, Labrador, Norway, the British LITH FORMERS IN TROPICAL TO ARCTIC Isles, Atlantic France, and Spain). In clearer WATERS WITH GENERAL DEPTH OF OCCURRENCE waters, rhodoliths can occur deeper and will be found near the photic limit in the larger bays Location Depth Species and even on exposed coast (for example, New- foundland and northwest Norway). In very Arctic to Shallow Lithothamnium clear tropical waters, rhodoliths can occur on lemoineae offshore banks and in exposed localities in subarctic Shallow to Lithothamnium depths of 50 to 200 m. However, even in pro- deep glaciale Deep tected tropical lagoons, they may still be rela- Lithothamnium tophiforme tively abundant. Temperate to Shallow to Phymatolithon In summary, open-structured, free-branch- subtropical deep calcareum Lithothamnium ing rhodoliths (maerl) can occur from shallow coralloides (0 to 10 m) to deep ( >40 m) water, depending Lithophyllum on the species and exposure, and from the byssoides arctic to the tropics. Several examples are given Tropical Shallow Neogo nio lithon in Table 6. Although massive, concentrically strictum Shallow Lithophyllum banded, rhodoliths are generally associated with pallescens deep tropical waters, somewhat similar rhodo- Deep Archeolithothamnium liths formed by Archeolithothamnium eryth- timorense raeum, Hydrolithon reinboldii, and Tenarea sp. ate known from shallow Pacific waters. Also, factors controlling distribution are tempera- Phymatolithon polymorphum forms large free ture control of reproduction and growth, and nodules in deep water on the northern Nor- light control of photosynthesis and growth wegian coast, although these are generally (Adey, 1970b). With the increasing emphasis on hollow. modern carbonate productivity studies in Thus, in view of present data on rhodoliths, various marine environments, greater caution rhodolith morphology should not be related must be used in dealing with crustose coralline to energy conditions beyond the observation algae, particularly if valid budget calculations that a massive nodule probably is characteristic are to be made. Turnover rates, for example, of a higher energy situation than a large open cannot be established with scant knowledge of brancher. Species do show a characteristic species and their growth rates, as previously surficial morphology which is largely dependent applied in this manner (Smith, 1970, p. 53-55). upon the factors of light, temperature, and Productivity studies must be based on adequate water motion. Bosellini and Ginsburg (1971) knowledge of both crustose coralline species described a relation between rhodolith form and their habitat condition:;. It was demon- and environment for Bermuda, but care should strated for example, in a study of several arctic- be taken in generalizing on this pattern until boreal species of the genera Phymatolithon- more information becomes available. Also of Leptophytum, that the deep- and shallow-water critical importance to the development and species had comparable optimum growth rates form of rhodoliths is the boring action of in the laboratory, although the plants were invertebrates. Perhaps arctic-boreal rhodoliths maintained at light intensities that differed are generally less dense than their tropical from one another by an order of magnitude counterparts owing to a low growth rate, as (Adey, 1970b). Temperature :.s another critical compared to a relatively high dissolution rate factor; data on both the recoided temperature by boring and scraping organisms. In addition, and the recent temperature rscord of crustose submarine lithification of sediment in internal corallines are essential in determining their cavities is of considerable importance in the existing growth rates (see Adey, 1970b). Fur- tropics but apparently negligible in the arctic. thermore, it should be noted that the growth A thorough study of rhodoliths and their rates of different tissues in the same plant may environments is required before critical paleo- vary, for perithallial rates in some species are ecological interpretations should be based on nearly comparable to hypothallial rates, where- their morphology. as in others, perithallial. rates may be several orders of magnitude lower than the hypothallial Reproductive and growth-rate studies on rates. Consequently, species, tissue, and growth several species have indicated that the primary Downloaded from http://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/84/3/883/3433487/i0016-7606-84-3-883.pdf by guest on 29 September 2021 CRUSTOSE CORALLINE ALGAE 901 rates versus light and temperature must all be angium. considered if valid turnover rates are to be Sporangia initial—the cells from which the established from limited experimental growth sporangium develops. rate studies. The same factors must be taken into account in studies of primary productivity REFERENCES CITED in crustose corallines (see, for example, Marsh, Adey, W. H., 1964, The genus Phymalolilhon in the 1970, where plants used were not identified to Gulf of Maine: Hydrobiologia, v. 24, p. 377- genus). Moreover, the subsequent results 420. should not be generalized for crustose coral- 1965a, Studies of Lithophyllum and related lines until more is known about the produc- algal genera: Colorado School Mines Quart., tivity of various tissues, species, and genera, v. 60, p. 1-105. relative to environmental conditions. 1965b, The genus Clathromorphum in the Gulf of Maine: Hydrobiologia, v. 26, p. 539- 573. ACKNOWLEDGMENTS 1966a, The distribution of saxicolous crustose Special thanks are extended to J. L. Wray corallines in the northwestern North Atlantic: (Marathon Oil Company) and R. N. Ginsburg Jour. Phycology, v. 2, p. 49-54. (University of Miami) who critically read the 1966b, The crustose corallines of the North original manuscript and offered suggestions for Atlantic: Am. Petroleum Inst. Rept., project no. 79, unpub. rept., 20 p. its improvement. L. B. Isham's assistance with 1968, The distribution of crustose corallines illustrations is gratefully acknowledged. on the Icelandic coast: Sci. Islandica (an- niversary volume 1968), p. 18-30. GLOSSARY 1970a, A revision of the Foslie crustose Conceptacle—a cavity in which the reproductive coralline herbarium: Norske Vidensk-Selsk. structures are developed. Skr. Kl„ v. 1, p. 1-46. Conceptacle cap—layer of varying thickness of 1970b, The effects of light and temperature vegetative cells above developing conceptacle, on growth rates in boreal-subarctic crustose typically breaking away as it matures. corallines: Jour. Phycology, v. 6, p. 269-296. Conceptacle primordium—layer of cells from which 1970c, Some relationships between crustose conceptacle develops. corallines and their substrate: Sci. Islandica, Epithallium—generally the tissue lying outside the v. 2, p. 21-25. lateral meristem and being produced from it. 1971, The sublittoral distribution of crustose Equivalent to cover cells. corallines on the Norwegian Coast: Sarsia, Fusion (of cells)—a relatively wide passage through v. 46 p. 41-58. the cell wall connecting cells of adjacent fila- Adey, W. H., and Adey, P. J., 1973, The crustose ments, apparently allowing the free com- corallines of the British Isles: British Phycolog. munication of cytoplasm. Jour, (in press). Heterocyst (Tricnocyte)—perithallial cell that is Adey, W. H., and Johansen, H. W., 1972, Mor- generally larger than surrounding cells. Com- phology and taxonomy of Corallinaceae with monly does not show the original hairlike projec- special reference to Clathromorphum, Meso- tion. phyllum and Neopolyporolithon, n. g.: Phyco- Hypothallium—the basalmost tissue in which the logia, v. 11, p. 159-180. filament(s) are oriented parallel to the substratum Adey, W. H., and Lebednik, P. A., 1967, Catalogue (basal hypothallium). Coaxial hypothallium: any of the Foslie Herbarium: Trondheim, Norge, kind of hypothallial tissue in which the cells are Det Kongelige Norske Videnskabers Selskab arranged in arched rows. Museet, 92 p. Meristem—region or cell layer in which most of the Adey, W. H„ and McKibbin, D. L., 1970, Studies vegetative cell division occurs. on the maerl species in the Ria de Vigo: Perithallium—thin or massive tissue lying between Botanica Marina, v. 8, p. 100-106. the hypothallium and the lateral meristem and Barnes, J., Bellamy, D. J., Jones, D. J., Whitton, composed of filaments oriented essentially per- B. A., Drew, E. A., and Lythgoe, J. N., 1970, pendicular to the substrate. Sublittoral reef phenomena of Aldabra: Secondary pit—pit connecting adjacent cells not Nature, v. 225, p. 268-269. belonging to the same filament. Barnes, J., Bellamy, D. J., Jones, D. J., Whitton, Sori—group of single sporangial compartments. B. A., Drew, E. A., Kenyon, L., Lythgoe, J. Sporangium—a cell which eventually produces one N., and Rosen, B. R., 1971, Morphology and or more spores. ecology of the reef front of Aldabra, in Stod- Sporangial cap—mucilaginous plug formed as part dart, D. R., and Yonge, M., eds., Regional of the sporangial wall and eventually filling the variations in Indian Ocean coral reefs: New pore in the conceptacle roof above the spor- York, Academic Press, p. 87-114. 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