what is hermatypic?

Coral Reefs (1985) 4:1 9 Coral Reefs �9 Springer-Verlag 1985

What is hermatypic? A redefinition of ecological groups in corals and other organisms

Helmut Schuhmacher and Helmut Zibrowius

Fachbereich 9 - Hydrobiologie, Universit~it GHS Essen, Postfach 103 764, D-4300 Essen, Federal Republic of Germany, and Universit6 d'Aix-Marseille 2, Centre d'Oc6anologie de Marseille (CNRS-URA41), Station Marine d'Endoume, Rue de la Batterie des Lions, F-13007 Marseille, France

Accepted 3 December 1984

Abstract. The term hermatypic, as widely used in the literature of extant and fossil Scleractinia, includes, by definition (Wells 1933), the confusing generalization of equating reef-building with containing zoox-anthellae. In course of time the use of the term diverged into denoting organisms which are either reef-building (including calcareous Rhodophyta) or those that contain zooxanthellae (including soft Alcyonaria). The equation: reef-building corals harbour zooxanthellae and vice-versa, is invali- dated by reviewing the various ecological categories of corals such as: reef-building species without the support of zooxanthellae, zooxanthellae-containing corals which inhabit but do not build reefs, zooxanthellae-containing, non-reef-building corals beyond the bathymetric and latitudinal limits of reefs, and framework-erecting corals in deep waters without zooxanthellae. Former attempts to improve the original definition of hermatypic are shown to be insufficient to match the ecological diversity of corals. A strict terminological separation of the properties zooxanthellae-containing, reef-building and (more generally) framework-building is provided by the use of the revised, respectively new terms zooxanthellate, hermatypic and constructional (with the respective anto- nyms azooxanthellate, ahermatypic and nonconstruc- tional). This terminology also applies to non-scleractinians.

Introduction

The terms hermatypic and ahermatypic are widely used in the literature of extant and fossil Scleractinia in order to distinguish between two main categories of corals. However, the student of corals or reefs will not find their meaning clearly explained in textbooks or dictionaries. He rather has to deduce the meaning from the respective context in the literature where the terms are bona fide passed on by the coral- and reef-workers community

since their creation by Wells (1933). Uncritical use has al- lowed the sense of these terms to diverge.

The great range of what is meant by hermatypic today may be illustrated here by an example from each end of the continuum. Goreau (1963) called algae such as Poro- lithon (calcareous Rhodophyta) which substantially contribute to the reef-framework, hermatypic. On the other hand, one also encounters expressions like hermatypic soft corals (Wainwright 1967). In the former case hermatypic means reef-bulding, in the second case hermatypic means containing zooxanthellae.

The reason for such a divergent use can be traced back to the little known text (Wells 1933) defining hermatypic and ahermatypic. In fact, from our modern point of view this definition itself is ambiguous; persistent uncritical and unmodified use of these older terms would mean a regression with respect to the more advanced knowledge of coral and reef ecology. A revision is therefore proposed to conform to the need for a precisely differ- entiating terminology.

Historical background

Early coral workers felt the necessity to distinguish between the reef-building scleractinians characteristic of shallow water environments in tropical seas and the other scleractinians. Altogether the latter were generally called "deep-sea corals", mainly because those that were really typical of deep water had been an object of special attention for the famous expeditions of the 19th century (Por- cupine, Challenger, Blake, Prince of Monaco etc.), which procured many new species, often from considerable depths, some hauls attaining or even exceeding 4,000 m. "Deep-sea corals" thus had become a misleading and generalized expression for all corals that were not reef- building and living under highly diversified environmental conditions. In fact, they are found from superficial water to great depths, and from the tropics to high latitudes (Zibrowius 1980; Cairns 1982). This wide range even includes typical reef-building corals in shallow

tropical water as the substrate of so-called "deep-sea corals".

At present the deepest record for a scleractinian coral is 6,300 m near the Aleutian trench (Keller 1976: Fungia- cyathus symmetrieus aleutieus, Vityaz star. 4120: 53~ 159~ 6,296-6,328 m). Maksimova's (1972) indica- tion of 10,710 m for a "solitary coral" in the Marianas trench is a mistake and refers to an actinian, not to a scleractinian species.

In a foot-note to a study of Cretaceous corals, Wells (1933, p. 109) criticized the term "deep-sea corals" then in general use and proposed the terms hermatypic and ahermatypic, as follows (here quoted in extenso): "The term deep-sea corals is unfortunate, because there is no real distinction between corals found in bathyal and neritic environments, with the exception of the true reef corals which are exclusively neritic. The term hermatypic, from herma, a reef, is therefore proposed to describe corals of the reef-building type, the living species of which possess symbiotic zooxanthellae within their tissues. In contrast to this term, ahermatypic is proposed to describe the corals of the non-reef-building type, the living forms of which live under greatly varying conditions of depth, temperature, and light. The use of these terms eliminates the inaccurate expression 'deep-sea corals'. Ahermatypic corals include both the deep (bathyal) and shallow (neritic) water forms which do not build reefs."

Unfortunately, two criteria which frequently but not necessarily coincide, are linked together in this definition: reef-building (that is, capability to erect a wave resistant skeleton), and the possession of zooxanthellae. Thereby Wells had anticipated the causal link between symbiotic algae and the potential of increased lime secretion in scleractinians, more than 20 years before it was experimentally demonstrated by Goreau and Goreau (1959).

A rather limited cryptic use was made of Wells' terms for about three decades. For instance, his terms are not referred to in either Yonge's (1940) fundamental article on the biology of corals or in his later review (1958). But it has been extensively used in a spreading reef literature. Simultaneously the meaning of the term hermatypic drifted apart, with quite confusing consequences.

The wide use of hermatypic in the literature

Since the 1960's the term hermatypic became common in the literature, but the unfortunate original equation of reef-building with containing zooxanthellae, was not conceptually separated. Up to the present it was concur- rently used to distinguish reef-building (and reef-inhabiting) corals from the non-reef-building (and non-reef-inhabiting) ones; shallow water corals from deep sea forms, tropical corals from those of high latitudes; and animals with zooxanthellae from those without such algal symbionts. This is illustrated by a few examples: The coe- lenterate volume of the Treatise on Invertebrate Paleon- tology provides two different explanations of the terms: in a "glossary of morphological terms applied to corals"

(Moore et al. 1956, pp. F245, F248) one finds hermatypic = reef-building, ahermatypic = not reef-forming, whereas Wells' contribution on the Scleractinia (1956, p. F353) reiterates the original definition implicating zooxanthellae.

Goreau (1963) again used hermatypic in the former sense of reef-building only, including calcareous Rhodo- phyta within the hermatypes. From this point of view the possession of zooxanthellae is not a prerequisite to call a species hermatypic, more important are its constructional abilities; in reef-building corals the zooxanthellae are just the physiological source for the higher frame- building potential.

Quite the contrary is understood by Wainwright (1967) who adopted the term hermatypic solely to denote the possession of zooxanthellae. He thus qualified gorgonians with dinoflagellate symbionts, including the "gorgonian family Xeniidae", as being hermatypic corals. Neither gorgonians nor the alcyonarian Xeniidae contribute to the reef frame-work; the latter ones even may impede corals in reef-building (Schuhmacher 1975). After death the colonies of these octocorals disintegrate to minute spicules which generally are widely dispersed by the currents (exceptions are alcyonarian spiculites described by Montaggioni 1980; and Konishi 1982). One of the more recent authors in this tradition is Stanley (1981, p. 509) who again arbitrarily reduced the meaning of hermatypic to containing zooxanthellae.

The imprecise extensions of Wells' terms are also evident when we trace the meaning of the antonym of hermatypic. Maragos (1974a) called the hard calcareous Tubastraea coecinea and Stylaster elegans as well as soft Sarcophyton and "other unidentified alcyonarians" (1974b) ahermatypic. Tubastraea, a scleractinian, and Stylaster, a hydrocoral, do not contain zooxanthellae; Sarcophyton, however, does; their common feature is that they do not contribute to the reef framework. On the other hand Mariscal and Bigger (1977) equated ahermatypic with not containing zooxanthellae, when they qualified the pennatularian Renilla as ahermatypic. The list of examples, where hermatypic is used to denote either reef- building or containing zooxanthellae, could by far be prolonged.

Still another interpretation was made by Beauvais (1973): she simply defined hermatypic corals as those which grow on reefs, a pragmatism understandable from the paleontologist's point of view (also underlying Wells' definition). But this oversimplification does not match the reality of various ecological groups in reefs.

Previous attempts to overcome the terminological confusion

Various coral and reef workers felt the need to adapt terms to the more complex reality. When writing on soft bottom corals such as Fungia, Diaseris, Cycloseris and Heteropsammia, Goreau and Yonge (1968, p. 421) ob- jected "It is paradoxical that all these forms belong to the

category of hermatypic (reef-building) corals, because they contain zooxanthellae. In an ecological sense, however, they are ahermatypic (non-reef-building), because their solitary free-living mode of life on muddy bottom precludes participation in the process of reef-building."

Buddemeier and Kinzie (1976, p. 185) clearly recognized the problem. They tried to end the confusion by separating the two senses inherent in Wells' term hermatypic. They strictly confined "hermatypic" to reef-building and defined symbiotic as containing zooxanthellae (antonym: non-symbiotic). In addition, they defined the useful term aposymbiotic for corals which usually contain zooxanthellae, but (temporarily) are free of them for some reason.

Their equation symbiotic = zooxanthellae-containing, however, reflects a too narrow view of what the animal host can harbour. For instance, the freshwater Chloro- hydra is symbiotic, but does not contain zooxanthellae. The general term symbiotic should rather be kept open to denote partnerships with different systematic groups, such as between the coral Fungia and its mytilid associate Fungiacava (Goreau et al. 1969) or the coral Heteropsam- mia and the sipunculid Aspidosiphon (Feustel 1966). Heteropsammia may even contain further symbionts, such as the mytilid Lithophaga (Arnaud and Thomassin 1976) or the ascothoracid Petrarca (Grygier 1981), and thus be "polysymbiotic". In both examples the scleractinians contain zooxanthellae, but they are peculiar for having still another or even more symbionts. Here it would be more appropriate to use the term "symbiotic" in order to discern these corals from others lacking such additional symbionts. This contrast may be illustrated by Cycloseris cyclolites (Lamarck 1801) and He teropsammia michelini (Milne Edwards and Haime 1848), both soft bottom inhabitants containing zooxanthellae, and of which only the latter is symbiotic with Aspidosiphon.

Ktihlmann (1984, p. 35) distinguishes between hermatypic (equated with reef-building) and symbiotic (equated with zooxanthellae-containing) and thereby separates four ecophysiological groups: (1) hermatypic-symbiotic, (2) hermatypic-aposymbiotic, (3) ahermatypic-symbiotic, (4) ahermatypic-aposymbiotic corals. Aposym- biotic is used by Kfihlmann in the sense of non-symbiotic of Buddemeier and Kinzie (see above).

Rosen (1981, p. 106) preferred to refer to the ecological categories of the tropical shallow-water reef-building corals and of the diversified non-reef-building corals as zooxanthellates and non-zooxanthellates, respectively. These terms have been expressively presented as equiva- lents to the hermatypes and ahermatypes of Wells and of "most other authors". The new terms were "especially in- tended to avoid ambiguities in a paleontological sense" (Rosen here apparently referred to the importance for paleontologists of distinguishing between deep and shallow water bioherms). Here again non-reef-building is equated with being devoid of zooxanthellae, and possess- ing zooxanthellae equated with contributing to the process of reef-building. Rosen's (1981) proposition seems to

overcome ambiguities as exemplified above by hermatypic calcareous Rhodophyta (Goreau 1963) and hermatypic xeniid soft corals (Wainwright 1967). However, the equation zooxanthellate = hermatypic again transfers the xeniids into an incorrect position.

The two categories hermatypic and zooxanthellate on one side and ahermatypic and non-zooxanthellate on the other cover the bulk of coral-phenotypes, but they are not sufficient to discern the ecological diversity of corals in the light of modern knowledge. In the following the link hermatypic - zooxanthellate (already criticized by Zibrowius 1982, p. 113) is questioned in a series of examples.

A reef-building coral without the support of zooxanthellae

A reef is a persistent, positive topographic biogen structure, rising up to the surface of the sea and characterized by its capability to resist hydrodynamic stress (e.g. Lowenstam 1950; Nelson et al. 1962; Braithwaite 1973; Heckel 1974; Schuhmacher 1976).

Hence several papers recently examined the mechanical properties of various corals, including zooxanthellate and azooxanthellate species, of the erect staghorn-type and of cushion-like growth (Chamberlain 1978; Tuni- cliffe 1979; Schuhmacher and Plewka I981 a, b; Schuhmacher 1981, 1984). The results generally show that the mechanical strength in branching forms (e.g. Acropora species) is superior to that in massive forms.

Among the branching forms Tubastraea micranthus (Ehrenberg 1834) is especially noteworthy for its extraor- dinary mechanical qualities. Although conventionally grouped with the ahermatypic corals because of the ab- sence ofzooxanthellae, this species equals or even surpas- ses the strongest hermatypic zooxanthellate corals, including well-recognized reef-builders as Acropora cervicornis (Lamarck 1816) and A.palmata (Lamarck 1816) (Schuhmacher 1984). T. rnicranthus occurs from the Red Sea to Madagascar and the Fiji Islands, and shows a considerable range in size and habitat requirements (Cross- land 1952; Schuhmacher 1984). The examined morph from Philippine reefs is frequent in 4-20 m depth, but not beyond 60 m, with rigid arborescent colonies rising up to 1 m above the bottom. The broadened and heavily calci- fied trunk provides a solid foothold against currents up to at least 1 m/s. Because of this mechanical strength 7". micranthus colonies were the only ones that remained erect in dynamite-blasted reefs.

By its structure and morphology T. micranthus fits well into the category of primary framework-builders as described by Goreau (1963) and Goreau and Goreau (1973). There would be no reason to exclude T.micranthus from the same functional group as the concurrent Acropora palifera (Lamarck 1816), A.formosa (Dana 1846) and similar eminent frame-builders, unless lack of zooxanthellae continues to be considered a decisive cri- terion.

In contrast to the ecological position of T. mieranthus is that of T. aurea (Quoy and Gaimard 1833), another azooxanthellate reef-inhabiting dendrophylliid; measure- ments of the skeletal properties do confirm its affiliation with non-reef-builders (Schuhmacher 1984).

Examples of non reef-building corals with zooxantheHae

Various zooxanthellate scleractinians are definitely not reef-building.

The situation in reef areas

Solitary free-living members of the Fungiidae, such as Diaseris distorta (Michelin 1843) and Cyeloseris sp. are to be found among seagrasses on sandy bottoms (Goreau and Yonge 1968; Pichon 1974; Gill and Coates 1977; Schuhmacher 1979). Other fungiid corals, occuring loosely dispersed among reef-building corals, conform best to the secondary hermatypes of Goreau (1963) and Goreau and Goreau (1973). The free-living soft bottom coral Heteropsammia is most literally ahermatypic, i.e. not reef-building. The zooxanthellate state is the rule in shallow water but specimens from 50 m depth at Reunion Island were found devoid of zooxanthellae.

The situation beyond the latitudinal reef limit

Zooxanthellate scleractinians are not restricted to the tropics. Up to now our knowledge of typical extratropical zooxanthellate corals is restricted to the eastern and western North Atlantic and to the Mediterranean Sea. But it can be expected that extratropical zooxanthellate forms (other than species known from reefs, but extend- ing locally to exceptionally high latitudes) do exist, too, in the northern Pacific and in the southern hemisphere.

On the Atlantic coast of North America the colonial shallow-water coral Astrangia astraeiformis Milne Ed- wards and Haime 1849 has its northern limit on the coast of Massachusetts. It occurs naturally with or without zooxanthellae (Szmant-Froelich and Pilson 1980; Cairns 1981).

In the northeastern Atlantic and the Mediterranean five zooxanthellate species have been found, far away from any coral reef area (Zibrowius 1980). Madracis as- perula Milne Edwards and Haime 1849 occurs in the Cape Verde Islands, Canary Islands and the Madeira archipelago. It forms rather large encrusting zooxanthellate colonies under euphoric conditions and slender branching zooxanthellae-free colonies in obscure environments such as caves and deeper overhangs. In the Mediterranean Madraeispharensis (Heller 1864) has been found without zooxanthellae in obscure caves, and with zooxanthellae on well-lit overhangs and cliffs; both forms are of the same encrusting type without branches.

The faviid Cladoeora caespitosa (Linnaeus 1767), widespread throughout the Mediterranean, has always been found in possession of zooxanthellae. The symbionts have been mentioned in the literature as early as 1882 (Heider, p. 657) although their true nature has not been recognized at the time. This is a very variable species with a wide ecological range under euphotic conditions. By its frequently large-sized colonies and local abun- dance it comes rather close, ecologically, to tropical reef- building corals.

Balanophyllia europaea (Risso 1826) is a solitary zooxanthellate dendrophylliid typical of the Mediter- ranean. According to Duclaux and Lafargue (1973) zooxanthellae-free specimens do exist. This assertion appears in contradiction with experimental results of Zibrowius: Specimens transplanted at Marseille into the dark (caves) lost their zooxanthellae and died after some weeks.

Oeulina patagoniea De Angelis 1908 was found in some localities in the Ligurian Sea and at the southeast- ern coast of Spain (Zibrowius 1974; Zibrowius and Ramos 1983). It has been recognized as a rather recent accidental immigrant from extratropical South America (northern Argentina to southern Brazil), where it is mainly known as a Pleistocene fossil. The colonisation strategy is typical for an invader: the species is particularly abundant in extreme environments uncommon for a scleractinian, such as polluted harbours and rocks ex- posed among sand at shallow depth. In full light the colonies are fast growing but they do not depend entirely on their zooxanthellae. Placed into a dark cave they lost their symbionts, but survived for 29 months; after re- transplantation into full light the apozooxanthellate colonies reestablished the symbiosis and took on the dark brown colour of normal zooxanthellate colonies.

The situation at the reef base

Especially revealing for our problem is also the transient zone between the living reef and the aphotic depths. The reef as habitat and structure is characterized by an inter- play of various growthforms which create projecting and space-enclosing structures. The resulting framework harbours a proper biocoenosis before it is gradually filled in by calcareous deposits. On the basis of an extensive submersible survey of the upper 200 m of the coastal slope in the Gulf of Aqaba, Fricke and Schuhmacher (1983) showed how the three-dimensional, erect or hemispheri- cal growth forms of light-dependent reef corals change with increasing depth into low-relief crusts. With decreasing light intensity they no longer create a typical reef structure but rather a different facies as already noticed by Vaughan and Wells (1943, p. 52). The flattened colonies are no more constructional in the sense of forming a three dimensional calcareous meshwork, and the inhabiting biocoenosis is altered and depauperate, com- pared to the former one.

Although zooxanthellate corals continue to form ex- tended communities at the reef base, they are unable to rise considerably above the surrounding bottom due to the reduced calcification rate (Goreau 1963). The depth where the growth of skeletal material just balances the loss due to physical and - predominantly - biological agents, can be regarded as compensation depth for reef growth (Schuhmacher 1983). It depends not only on the ambient light but also on the slope morphology. The compensation depth for reef growth is considerably above the photosynthetic compensation depth of zooxanthellate corals which is determined by the balance of photosynthetic assimilation and respiration. In the very transparent waters of the Gulf of Aqaba it lies at about 100 m depth and thereby compares well with data from the Caribbean and Pacific (Fricke and Schuhmacher 1983). The compensation depth for reef growth, however, does not exceed 60 m.

The coral community between the reef base and the photosynthetic compensation depth is composed of species that are hermatypic in the strict sense (= reef-building) a couple of meters above, and of a few - also zooxanthellate - species that exclusively occur at the reduced light conditions of the deeper forereef such as Leptoseris tenuis Van der Horst 1921, and L.fragilis Milne Edwards and Haime 1849. L.gardineri Van der Horst 1921, also occurs in shallow depths elsewhere (Veron and Pichon 1980). Leptoseris fragilis is noteworthy because of its especially deep range from 100 to 145 m (Fricke and Schuhmacher 1983), which is below the photosynthetic compensation depth. The physiology of this coral deserves further study. L.fragilis and other exclusively low light adapted species (zooxanthellate but definitely not hermatypic) are characterized by fragile skeletons.

The decreasing constructional importance of zooxanthellate corals with increasing depth is due to the di- minished calcification rate and the flattening of the colony geometry. Corals devoid of zooxanthellae, need not adapt their growth form to the light regime, but - as entirely heterotrophic organisms - rather should opti- mize their plankton-catching abilities.

In fact, below 100 m in the Gulf of Aqaba, the zooxanthellae-free species Madracis interjecta Marenzeller 1907 and Dendrophyllia cf. minuseula Bourne 1905, form arborescent colonies (Fricke and Hottinger 1983; Fricke and Schuhmacher 1983). Aggregated, their colonies pro- vide the frame for subsequently settling scleractinians, fo- raminiferans, bryozoans and serpulids, and also trap sed- iment. These hardbottom structures rise more than 1 m above the bottom and, by definition, are bioherms - not to be confounded with the reef which is confined to depths close to the water surface (Cumings 1932; McNeil 1954; Braithwaite 1973; Schuhmacher 1976). The species initiating the deep-water bioherms of the Gulf of Aqaba presumably grow too slowly to cope with the hydrodynamic stress near the water surface. They all lack the skeletal strength and morphological adaptions which enable Tubastraea micranthus to colonize the reef.

At Jamaica coralline sponges - hard skeleton-de- positing Porifera without zooxanthellae - are found to contribute locally to the framework of the deeper forereef. Ceratoporella nicholsoni Hickson 1911, the most conspicuous species with individual sizes exceeding 1 m in diameter, occurs from 30-300 m. Between 74 and 98 m it covers 25%-50% of the surface beneath ledges and in large caves (Hartman and Goreau 1970; Lang et al. 1975). The strength of its aragonitic skeleton is superior to that of zooxanthellate Scleractinia which prompted the speculation that frame-builders of ancient times became hermatypic by other means than enhancing skeletal growth by pace-making zooxanthellae (Schuhmacher and Plewka 1981 a).

Corals constructing deep-water bioherms, worldwide

There is a considerable variety of deep-water bioherms essentially constructed by colonial branching scleractinians. The frame-builders of the deep-water biotherms are ahermatypic, in the strict sense, being unable to contribute to reefs. Their formative role should be recognized by the term "constructional". The classical case is the Lo- phelia banks, originally described by Scandinavian authors from the Norwegian fjords. Geologists are in- creasingly aware that coral bioherms occur not only in warm shallow seas (the tropical coral reefs), but also in deep and cold water; a distinction which deserves close attention for the environmental interpretation of ancient coral formations (Teichert 1958; Maksimova 1972). A short review, complementing a previous one by Cairns and Stanley (1982), shows the diversity of constituents and the wide geographic range of deep-water bioherms in the present fauna:

In the northeastern Atlantic three species are important constructors: Madrepora oculata Linnaeus 1758, Lo- phelia pertusa (Linnaeus 1758) [= L.prolifera (Pallas 1766)], and Solenosmilia variabilis Duncan 1873. The role of L.pertusa has been known for a long time because of its occurence in relatively shallow water (starting with 60-80 m) in Norwegian fjords. Extension and development of patches of this species have been investigated by Wilson (1979a, b) who also used submersible observations on Rockall Bank. Knowledge of the role ofS. variabilis as a third important constructor is quite recent (Zi- browius 1980); previously this species had not always been distinguished from the two others.

All three species, M. oculata, L.pertusa, and S. variabilis, are widespread in the Atlantic, Indian and Pacific oceans (Zibrowius 1980; Cairns 1979, 1981, 1982) and locally may be major constituents of deep water coral banks. At least this has been confirmed for L.pertusa in the northwestern Atlantic, and for S. variabilis in the northwestern Indian Ocean (Alcock 1898 as S.jeffreyi) and southern Pacific (Cairns 1982; Cairns and Stanley 1982).

In the northwestern Atlantic deep-water coral banks are known similar to those in the northeastern Atlantic,

with Enallopsammia profunda (Pourtal6s 1867) being another major constituent, in addition to Lophelia pertusa. These structures have been reported, notably, from the Blake Plateau and the Straits of Florida (Cairns and Stanley 1982). Azooxanthellate Oculina varicosa Lesueur 1820, constitutes the framework of coral thickets on the Central East Florida coast (Reed 1980, 1982) in lesser depths (70-100m) than L.pertusa and E.profunda. O. varicosa occurs as discrete zooxanthellate colonies in shallow water.

Goniocorella dumosa (Alcock 1902) has a wide distribution throughout the Indo-West-Pacific, from Japan to New Zealand and South Africa (collected off Natal on Meiring Naude cruises). In the New Zealand area it is known as the major constituent of deep-water coral banks (Cairns 1982), but its role as a constructor may not be limited to that area.

Coral bioherms below the euphotic zone (120-200 m) in the northern Red Sea (Gulf of Aqaba) are known from a submersible survey and consist essentially of Madracis interjecta Marenzeller 1907 and Dendrophyllia cf. minuscula Bourne 1905 (Fricke and Hottinger 1983; Fricke and Schuhmacher 1983).

Pseudocolonial Desmophyllum cristagalli Milne Ed- wards and Haime 1848, in fact a solitary non-budding species of world-wide distribution, has been reported as the framework of deep-water coral banks from the New Zealand area and from off Chile (Cairns 1982; Cairns and Stanley 1982). Similar dense formations of D. cristagalli are typical of the Pleistocene Mediterranean in great depths characterized by lower water temperatures than the present temperature of about 13 ~ Big clumps of Pleistocene D. cristagalli have been dredged and dense populations have been observed on submersible dives in various areas at depths of about 2,000 m (Zibrowius 1980, 1981).

Proposal for a revised terminology

The case-studies and review were given to demonstrate the conceptual short-comings of the previous ecological categorization of scleractinians and other reef-building organisms. In order to overcome this situation a revised terminology is proposed. The necessary supplements to Wells' definition are chosen as concisely as possible and with the attempt not to change the meaning of estab- lished terms.

I A Zooxanthellate: living in symbiosis with dinoflagellate

algae, usually Gymnodinium microadriaticum (Freu- denthal 1962).

B Azooxanthellate: without those symbionts [the prefix "a" is preferred to non-zooxanthellate, since it accen- tuates the lack of symbionts and goes parallel to the last pair of terms (III, below)]. The separation between zooxanthellate and azooxanthellate does not necessarily coincide with a separation of species. In fact, some species comprise zooxanthellate and azooxanthellate

C

II A

individuals or colonies, and can even be transformed, experimentally, from one into the other. Apozooxanthellate: may be used for organisms which usually contain zooxanthellae, but (temporarily) are free of them for some reason (hitherto called aposymbiotic).

Constructional: forming a bioherm, i.e. an elevated durable carbonate structure in shallow or deep water. Constructional forms are not necessarily hermatypic, but hermatypic forms are always constructional, as the reef represents one type of bioherm.

B Non-constructional: not forming such a structure.

III A Hermatypic: significantly contributing to the frame-

work of reefs (for definition see p. 3). All hermatypic forms are constructional.

B Ahermatypic: not significantly contributing to the framework of reefs. The separation between hermatypic and ahermatypic is not a clear cut one. Arbitrary classification cannot be ruled out. Which species have to be considered as significant contributors to the reef construction, and which species do not fulfill this con- dition often requires a subjective decision. In addition, the ecological role of a species may not be the same in different parts of its geographical area. Likewise, the distinction of primary and secondary hermatypes as proposed by Goreau and Goreau (1973) cannot be an absolute one.

Framework is understood as described by Lowenstam (1950), Ginsburg and Lowenstam (1958) and Goreau and Goreau (1973). The terms defined above do not denote a bathymetric classification. Shallow and deep- water corals should be designated as such. The limit between shallow and deep water is determined physio- logically as the photosynthetic compensation depth.

The listed terminology matches Wells' definition as long as hermatypic has been used in its primary etymo- logical sense (greek herma= rib, reef). The term ahermatypic is particularly useful for characterizing shallow water forms in reef areas. It is self-evident that deep- water constructional forms are ahermatypic, and cannot be hermatypic, reefs being - by definition - confined to shallow water. It is even a pleonasm to qualify deep- water corals as ahermatypic.

The term constructional became necessary as a some- what higher generic term to denote the capability of corals living in deep water and high latitudes to form thickets, banks or other kinds of bioherms which are not to be confused with reefs.

After a clear distinction has been made between hermatypic and zooxanthellate, there is no reason, why these terms should not be applied to non-scleractinians. For instance, the significance of calcareous Rhodophyta in es- tablishing the coral reef structure is reflected in the term "coralgal reef". In the marginal zone of the global coral reef belt and beyond are reef-like structures which de-

Table 1. Examples of the different ecological groups

Species Occurrence Zooxanthellate or Constructional or Hermatypic or azooxanthellate non-constructional ahermatypic

Non-Scleractinia Porolithon onkodes (Heydrich

1897) - Rhodophyta Ceratoporella nicholsoni

(Hickson 1911) - Sclerospongia Aglaophenia cuppressina

Lamouroux 1816 - Hydroidea Errinopsis reticulum

Broch 1951 - Hydroidea Millepora dichotoma

Forskfil 1775 - Hydroidea Cassiopea xamachana

Bigelow 1892 - Scyphozoa Heliopora coerulea (Pallas 1766) -

Coenethecalia Xenia species - Alcyonaria Anemonia sulcata (Pennant 1777) -

Actiniaria Tridacna species - Bivalvia Dendropoma species - Gastropoda

Scleractinia

Acropora formosa (Dana 1846) - Acroporidae

Leptoserisfragilis Milne Edwards and Haime 1849 - Agariciidae

Diaseris distorta (Michelin 1843) - Fungiidae

Fungiafungites (Linnaeus 1758) - Fungiidae

Fungiacyathus fragilis G. O. Sars 1872 - Fungiidae

Cladocora caespitosa (Linnaeus 1767) - Faviidae

Oculina varicosa Lesueur 1820 - Oculinidae

Lophelia pertusa (Linnaeus 1758) - Caryophylliidae

Balanophyllia europaea (Risso 1826)- Dendrophylliidae

Dendrophyllia cf. minuscula Bourne 1905 - Dendrophylliidae

Leptopsammia pruvoti Lacaze- Duthiers 1897 - Dendrophylliidae

Heteropsammia michelini Milne Edwards and Haime 1848 - Dendrophylliidae

Tubastraea micranthus (Ehrenberg 1834) - Dendrophylliidae

Tubastraea aurea (Quoy and Gaimard 1833)- Dendrophylliidae

Tropical Indo-Pacific, shallow Azooxanthellate Constructional Hermatypic

Tropical West Atlantic, shallow Azooxantheltate Constructional Ahermatypic (in caves), deep (forereef)

Tropical West-Pacific, shallow Zooxanthellate Non-constructional Ahermatypic

Subantarctic West Atlantic, deep Azooxanthellate Constructional Ahermatypic"

Tropical Indo-West Pacific, Zooxanthellate Constructional Hermatypic shallow

Tropical West Atlantic, Zooxanthellate Non-constructional Ahermatypic shallow


Tropical Indo-West Pacific, shallow Zooxanthellate Non-constructional Ahermatypic Mediterranean Sea, East Atlantic, Zooxanthellate Non-constructional Ahermatypic"

shallow Tropical Indo-West Pacific, shallow Zooxanthellate Constructional b Hermatypic b Tropical-subtropical Azooxanthellate Constructional (Locally)

West Atlantic, shallow hermatypic


Red Sea, Indian Ocean, deep Zooxanthellate Non-constructional Ahermatypic"

Tropical Indo-West Pacific, Zooxanthellate Non-constructional Ahermatypic shallow

Tropical Indo-West Pacific, Zooxanthellate Constructional b Hermatypic b shallow

Atlantic, deep Azooxanthellate Non-constructional Ahermatypic ~

Mediterranean Sea, Northeast Zooxanthellate Constructional Ahermatypic a Atlantic, shallow

Tropical-subtropical West Atlantic, Zooxanthellate Constructional Ahermatypic shallow-deep azooxanthellate

Atlantic, Mediterranean Sea, Azooxanthellate Constructional Ahermatypic a deep

Mediterranean Sea, shallow Zooxanthellate Non-constructional Ahermatypic"

Red Sea, Indian Ocean, deep Azooxanthellate Constructional Ahermatypic"

Mediterranean Sea, East Atlantic, Azooxanthellate Non-constructional Ahermatypic" shallow-deep

Tropical Indo-West Pacific, Zooxanthellate Non-constructional Ahermatypic" shallow-deep azooxanthellate

Red Sea, Indo-West Pacific, Azooxanthellate Constructional Hermatypic% shallow ahermatypic ~

Tropical Atlantic and Azooxanthellate Non-constructional Ahermatypic Indo-Pacific, shallow

a Formally ahermatypic - species does not occur in reefs b Secondary hermatypic in the sense of Goreau and Goreau (1973) c Hermatypic in the Philippines, ahermatypic in the Red Sea (Schuhmacher 1984)

serve special a t t en t ion wi th r ega rd to ou r p rob l em. The algal cup-reefs o f B e r m u d a (Verri l l 1906; G i n s b u r g and Schroeder 1973) a n d the reef-s t ructures a t F e r n a n d o de N o r o n h a I s l and and a long the Braz i l ian coas t (Branne r 1904; K e m p f and Labo re l 1968; Labo re l 1969) - to give on ly a few examples - a re no t erected by zooxan the l l a t e

o rgan i sms b u t by ca lcareous R h o d o p h y t a a n d vermet id gas t ropods . The conce rned species o f Neogoniolithon, Porolithon and Dendropoma ecologica l ly be long to the he rmatypes .

The concep tua l sho r t comings o f the t e r m i n o l o g y pre- v ious ly in use a re caused by ming l ing three ecologica l cat -

egories (distinguished above as I-III) in one term "hermatypic". Hence, a three-way designation is proposed to differentiate the ecological groups of frame-building and/ or zooxanthellae-containing species. Examples are given in Table 1.

The three pairs of characters in Table 1 can formally be combined in six permutations. In nature, however, only five combinations occur. The combination azooxanthellate/hermatypic/non-constructional does not exist, the characters hermatypic and non-constructional being inconsistent with each other. The proposition of a bundle of explicit terms reflects the differentiated ecological po- sitions &corals and other organisms. Hopefully it will improve the articulation and communication in a rapidly specializing field of research.

Acknowledgements. The authors are grateful to S. D. Cairns for the inter- est he has taken in the previous stages of the present paper and for his valuable suggestions.

References

Alcock A (1898) An account of the deep-sea Madreporaria collected by the Royal Indian marine survey ship "Investigator". Trustees of the Indian Museum, Calcutta

Arnaud PM, Thomassin BA (1976) First records and adaptive signifi- canoe of boring into a free-living scleractinian coral (Heteropsam- mia miehelini) by a date mussel (Lithophaga lessepsiana). Veliger 18:367-374

Beauvais L (1973) Upper Jurassic hermatypic corals. In: Hallam A (ed) Atlas of palaeobiogeography. Elsevier, Amsterdam, pp 317-328

Braithwaite C JR (1973) Reefs: just a problem of semantics? Am Assoe Petrol Geol Bull 57:1100-1116

Branner JC (1904) The stone reefs of Brazil. Bull Mus Comp Zool Harv Upiv 44:1-285

Buddemeier RW, Kinzie RA (1976) Coral growth. Oceanogr Mar Biol Ann Rev 14:183-225

Cairns SD (1979) The deep-water Scleractinia of the Caribbean Sea and adjacent waters. Stud Fauna Curagao 57:1-341

Cairns SD (1981) Marine flora and fauna of the Northeastern United States. Scleractinia. NOAA Techn Rep NMFS 438:1-14

Cairns SD (1982) Antarctic and subantarctie Scleractinia. Antarct Res Set 38:61-164

Cairns SD, Stanley GD (1982) Ahermatypic coral banks: living and fossil counterparts. Proc 4th Int Coral Reef Syrup 1:611-618

Chamberlain JA Jr (1978) Mechanical properties of coral skeleton: com- pressive strength and its adaptive significance. Paleobiology 4:419- 435

Crossland C (1952) Madreporaria, Hydrocorallinae, Heliopora and Tubipora. Sci Rep Great Barrier Reef Exped 1928-1929, Brit Mus (Nat Hist) 6:85-257

Cumings ER (1932) Reefs or bioherms? Geol Soc Am Bull 43:331-352 Duclaux G, Lafargue F (1973) Madr6poraires de M6diterran6e occiden-

tale. Recherche des Zooxanthelles symbiontiques. Compl6ments morphologiques et 6cologiques. Vie Milieu Set A 23:45-63

Feustel H (1966) Anatomische Untersuchungen zum Problem der Aspi- dosiphon-Heterocyathus-Symbiose. Verb Dtsch Zool Ges 1965:131- 143

Fricke HW, Hottinger L (1983) Coral bioherms below the euphoric zone in the Red Sea. Mar Ecol Progr Ser 11:113-117

Fricke HW, Schuhmacher H (1983) The depth limits of Red Sea stony corals: an ecophysiological problem (a deep diving survey by submersible). PSZN I: Mar Ecol 4:163-194

Gill GA, Coates AG (1977) Mobility, growth patterns and substrate in some fossil and recent corals. Lethaia 10:119-134

Ginsburg RN, Lowenstam HA (1958) The influence of marine bottom communities on the depositional environment of sediments. J Geol 66:310-318

Ginsburg RN, Schroeder JH (1973) Growth and submarine fossilization of algal cup reefs, Bermuda. Sedimentology 20:575-614

Goreau TF (1963) Calcium carbonate deposition by coralline algae and corals in relation to their roles as reefbpilders. NY Acad Sci Ann 109:127-167

Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239-250

Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs. II. Geomorphology, zonation, and sedimentary phases. Bull Mar Sci 23:421-432

Goreau TF, Younge CM (1968) Coral community on muddy sand. Na- ture (London) 217:421-423

Goreau TF, Goreau NI, Soot-Ryen T, Yonge CM (1969) On a new com- mensal mytilid (Mollusca: Bivalvia) opening into the coelenteron of Fungia scutaria (Coelenterata). J Zool 158:171-195

Grygier MJ (1981) Petrarca okadai, a new crustacean (Maxillopoda: As- cothoracica) from the Great Barrier Reef, the first shallow water record of the genus. Crustacean Biol 1:183-189

Hartman WD, Goreau TF (1970) Jamaican coralline sponges: their morphology, ecology and fossil relatives. Syrup Zool Soc London 25:205-243

Heckel PH (1974) Carbonate buildups in the geological record: a review. In: Laporte LF (ed) Reefs in space and time. SEPM Spec Publ 18:90-154

Heider A von (1882) Die Gattung Cladocora Ehrenb. Sitzungsber K Akad Wiss Math Naturwiss K1 1881 84:634-667

Keller NB (1976) The deep-sea madreporarian corals of the genus Fun- giacyathus from the Kurile-Kamchatka, Aleutian trenchs and other regions of the world ocean [in Russian, with English summary]. Trudy Inst Okeanol Akad Nauk SSSR 99:31-44

Kempf M, Laborel J (1968) Formations de vermets et d'algues calcaires sur les c6tes du Br6sil. Reel Trav Stn Mar Endoume-Marseille 59 (Bull 43):9-23

Konlshi K (1982) Alcyonarian spiculite: limestone of soft corals. Proc 4th Int Coral Reef Symp 1:643-649

Kiihlmann D (1984) Das lebende Rift. Landbuch Verlag, Hannover Laborel J (1969) Les peuplements de madr6poraires des e6tes tropicates

du Br6sil. Ann Univ Abidjan Ser E 3:1-261 Lang JC, Hartman WD, Land LS (1975) Sclerosponges: primary frame-

work constructors on the Jamaican deep fore-reef. J Mar Res 33:223-231

Lowenstam HA (1950) Niagaran reefs of the Great Lakes area. J Geol 58:430-488

Maksimova SV (1972) Coral reefs in the Arctic and their paleogeo- graphical interpretation. Int Geol Rev 14:764-769

Maragos JE (1974a) Reef corals of Fanning Island. Pac Sei 28:247-255 Maragos JE (1974b) Coral communities on a seaward reef slope, Fan-

ping Island. Pac Sci 28:257-278 Mariscal RE, Bigger CH (1977) Possible ecological significance of oc-

tocoral epithelial nltrastructure. Proc 3rd Int Coral Reef Symp 1:127-133

McNeil FS (1954) Organic reefs and banks and associated detrital sediments. Am J Sci 252:385-401

Montaggioni L (1980) Alcyonarian spiculites in coral reefs. 26e Congr G6ol Int Paris 2:521

Moore RC, Hill D, Wells JW (1956) Glossary of morphological terms applied to corals. In: Moore (ed) Treatise on invertebrate paleontology, pt F: Coelenterata. Geological Society of America, New York; University of Kansas Press, Lawrence, pp F245-251

Nelson HF, Brown CW, Brineman JH (1962) Skeletal limestone classification. Am Assoc Petrol Geol Mem 1:224-252

Pichon M (1974) Free-living scleractinian coral communities in the coral reefs of Madagascar. Proc 2nd Int Coral Reef Syrup 2:173-181

Reed JK (1980) Distribution and structure of deep-water Oculina varieosa reefs off Central Eastern Florida. Bull Mar Sci 30:667- 677

Reed JK (1982) In situ growth rates of the scleractinian coral Oculina varicosa occurring with zooxanthellae on 6 m reefs and without on 80 m banks. Proc 4th Int Coral Reef Symp 2:201-206

Rosen BR (1981) The tropical high diversity enigma - the corals' eye view. In: Forey PL (ed) Chance, change and challenge. The evolving biosphere. British Museum (Nat Hist), London; Cambridge Uni- versity Press, Cambridge, pp 103-129

Schuhmacher H (1975) Die Rolle der Weichkorallen (Alcyonacea, Octo- corallia) innerhalb der Riffbioz6nosen des Roten Meeres und des australischen GroBen Barriereriffs. Verb Dtsch Zool Ges 1974:380- 384

Schuhmacher H (1976) Korallenriffe. Bayerischer Landwirtschaftsver- lag, Miinchen

Schuhmacher H (1979) Experimentelle Untersuchungen zur Anpassung von Fungiiden (Scleractinia, Fungiidae) an unterschiedliche Sedi- mentations- und Bodenverh~iltnisse. Int Rev Gesamten Hydrobiol 64:207-243

Schuhmacher H (1981) Die Festigkeit von Korallenskeletten - ein bisher unbeachteter Parameter beim Riffaufbau. Verb Dtsch Zool Ges 1981:154

Schuhmacher H (1983) Die Tiefenverbreitung lichtabh~ingiger Steinko- rallen und die Ansatztiefe rezenter Rifle im Golf yon Akaba (Rotes Meer). Essen Geogr Arb 6:59-69

Schuhmacher H (1984) The reef-building properties of Tubastraea micranthus (Scleractinia, Dendrophylliidae), a coral without zooxanthellae. Mar Eeol Prog Ser 20:93-99

Schuhmacher H, Plewka M (1981 a) Mechanical resistance of reef- builders through time. Oecotogia (Berlin) 49:279-282

Schuhmacher H, Plewka M (1981 b) The adaptive significance of mechanical properties versus morphological adjustments in skeletons of Acropora palrnata and Acropora cervicornis (Cnidaria, Scleracti- nia). Proc 4th Int Coral Reef Symp 2:121-128

Stanley GD (198 I) Early history of scleractinian corals and its geological consequences. Geology 9:507-511

Szmant-Froelieh A, Pilson MEQ (1980) The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition ofAstrangia danae Milne Edwards & Haime, 1849. J Exp Mar Biol Ecol 48:85-97

Teichert C (1958) Cold- and deep-water coral banks. Am Assoc Petrol Geol Bull 42:1064-1082

Tunnicliffe V (1979) The role of boring sponges in coral fracture. Colloq Int CNRS 291:309-315

Vaughan TW, Wells JW (1943) Revision of the suborders, families and genera of the Scleractinia. Geol Soc Am Spec Pap 44:1-363

Veron JEN, Pichon M (1980) Scleractinia of Eastern Australia. III. Families Agariciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophyl- liidae. Aust Inst Mar Sci Monogr Set 4

Verrill AE (1906) The Bermuda Islands. IV. Geology and paleontology. V. An account of the coral reefs. Trans Conn Acad Arts Sci 12:45- 348

Wainwright SA (1967) Diurnal activity of hermatypic gorgonians. Na- ture (London) 216:1041

Wells JW (1933) Corals of the Cretaceous of the Atlantic and Gulf coastal plains and western interior of the United States. Bull Am Paleontol 18:85-288

Wells JW (1956) Scleractinia. In: Moore RW (ed) Treatise on invertebrate paleontology, pt F: Coelenterata. Geological Society of America, New York; University of Kansas Press, Lawrence, pp F328-F444

Wilson JB (1979a) The distribution of the coral Lophelia pertusa (L) [L. prolifera (Pallas)] in the north-east Atlantic. J Mar Biol Assoc UK 59:149-164

Wilson JB (1979 b) "Patch" development of the deep-water coral Lophe- liapertusa (L) on Rockall Bank. J Mar Biol Assoc UK 59:165-177

Yonge CM (1940) The biology of reef-building corals. Sci Rep Great Barrier Reef Exped: 1928-29, Brit Mus (Nat Hist) 1:353-393

Yonge CM (1958) Ecology and physiology of reef-building corals. In: Buzzati-Traverso (ed) Perspectives in marine biology. Scripps Insti- tution of Oceanography, La Jolla, California, pp I 17-135

Zibrowius H (1974) Oculinapatagonica, Scl~ractiniaire hermatypique in- troduit en M~diterran6e. Helgol Wiss Meeresunters 26:153-173

Zibrowius H (1980) Les Scl~ractiniaires de la M6diterran6e et de l'Atlan- tique nord-oriental. M6m Inst Oc6anogr Monaco I 1:1-284

Zibrowius H (1981) Thanatocoenose pl6istoc~ne profonde ~ Spongiaires et Scl6ractiniaires dans la Fosse Hell6nique. In: Journ6es d'6tudes sur la syst6matique 6volutive et la biog6ographie en M6diterran6e, Cagliari, 1980. Commission internationale pour l'exploration scien- tifique de la met M6diterran6e, Monaco, pp 133-136

Zibrowius H (1982) Deep-water scleractinian corals from the south- western Indian Ocean with crypts excavated by crabs, presumably Hapalocarcinidae. Crustaceana 43:113-120

Zibrowius H, Ramos AA (1983) Oculinapatagonica, Scl~ractiniaire exo- tique en M6diterran6e - nouvelles observations dans le Sud-est de l'Espagne. Rapp Comm Int Mer M6dit 28:303-306

what is hermatypic?

Documents