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Endolithic Fungi in Reef-Building Corals (Order: Scleractinia) Are Common, Cosmopolitan, and Potentially Pathogenic.

CHRISTOPHER J. BENTIS [*]

Reef-building corals appear to exist in dynamic equilibria with four principal partners: interconnected polyps of a colonial coelenterate, endosymbiotic dinoflagellate zooxanthellae residing in the host's endoderm, endolithic algae that penetrate coral skeletons, and endolithic fungi that attack both endolithic algae and the polyps. Although reports of fungal and algal-like endoliths in corals date back almost 150 years (1) and evidence of a fossil history extends as far back as the Upper Devonian ([sim]370 ma) (2), most attention has been paid to the structure (3), function (4, 5), and diversity (6) of the coral-zooxanthellae interactions, ignoring the endolithic members of the consortium. Recently, Le Campion-Alsumard et al. (1995) (7, 8) described an interrelationship between endolithic algae and fungi within the massive coral Porites lobata Dana 1846 (Poritidae), on Moorea island near Tahiti, French Polynesia. Fungi were also found to penetrate the most recently deposited skeletal material and to be asso ciated with pearl-like skeletal deposits formed by polyps of P. lobata in response to attack by their heterotrophic, endolithic symbionts. Here we extend these observations to the pocilloporid coral Pocillopora eydouxi and to the acroporid corals Acropora cytherea, Acropora humulis, and Montipora cf. studeri, collected at Johnston Atoll, central Pacific Ocean. Our observations suggest that direct coral-fun gal interaction is widespread, not only geographically, but taxonomically as well. Thus, fungal endoliths, acting as opportunistic pathogens, may play a greater role in the ecology of coral reef systems than previously recognized.

The oligophotic, siphonal green alga Ostreobium quekettii is ubiquitous in skeletons of live corals (9, 10). It is also common in other carbonate substrates, including dead shells and limestone, down to a depth of 300 m in clear waters of the Bahamas (11). Two other phototrophic organisms were reported from skeletons of live corals, the filamentous cyanobacterium Plectonema terebrans and conchocelis stages of bangiacean rhodophytes (12). Endolithic fungi in coral skeletons are equally common. They penetrate the corallum (euendolithic) and are often intermingled with endolithic algae, frequently parasitizing the latter (7). Fungi attack algal filaments by specialized hyphal branches, or haustoria, and often continue to grow inside algal filaments. Dense populations of algal and fungal endoliths have been associated with black-stained bands in specimens of P. lobata (13).

Although skeletons of dead corals are bored by a variety of endolithic microorganisms, there has been no evidence that endoliths can penetrate the layer of tissue that covers living coral surfaces, leading to the conclusion that infestation by a limited number of specialized endoliths occurs early in the life of a coral, and that endolithic algae and fungi continue to grow in parallel with the accretion of the corallum (8). Most filaments of O. quekettii and endolithic fungi extend in the direction of the axes of skeletal growth. In P. lobata, borings were detected in newly deposited skeletal spines (pali), demonstrating that the endoliths are able to keep up with the rates of skeletal accretion (7, fig. 2). The pearl-like skeletal deposits are always associated with fungal attacks during the residence of polyps in actively growing calicies. The polyps encapsulate the advancing hypha into dense repair aragonite, forming a distinct skeletal structure referred to as a "cone" (7).

The present study has two main objectives: to determine whether the relationship exhibited between P. lobata and endolithic fungi as described from the island of Moorea, in the eastern Pacific (7), and Mayotte, in the western Indian Ocean (13) exists in other corals, and if so, whether endolithic microboring fungi are able to keep pace with skeletal accretion rates and to interact with corals that exhibit rapid axial growth. The corals selected for study were Pocillopora eydouxi and Acropora cytherea. At Johnston Atoll, the mean ([pm] SD) annual growth rates of these corals (50.4 mm [y.sup.-1] [pm] 13.4, n = 16; and 93.21mm [y.sup.-1] [pm] 31.8, n = 21) are about 5 and 10 times that of P. lobata (13.1 mm [y.sup.-1] [pm] no data, n = 12), respectively (14). Distribution of endoliths and coral-fungal interactions were also investigated on selected specimens of Montipora cf. studeri and Acropora humulis. Ultimately, the purpose of our study was to determine whether endolithic fungi interact with corals on a bro ader taxonomic scale than previously recognized, and thus pose a potential threat to entire coral reef ecosystems.

Examination of A. cytherea and P. eydouxi in petrographic thin sections revealed the presence of algal and fungal endoliths, as well as the presence of cone-like protrusions on the surface of the corallum in both species. Conical structures were observed on walls and on septa of both axial and radial corallites in A. cytherea (Fig. lA, B) and on walls, septa, and spines of corallites in P. eydouxi (Figs. 1C, D; 2C, D). Fungal-coral interactions (cones) occurred regularly at the growth front of the colony in each of these species (Fig. lA, D). Cones were not evenly distributed on the surface of the corallum: they occurred either singly (Figs. 1A, B, D; 2B) or in clusters of several neighboring cones (Figs. 1C; 2A, C, D). Cones observed in this study were similar in both shape and size (Table 1) to those described for P. lobata (cf. 7). Each cone was penetrated by an axially positioned, unbranched fungal hypha (Fig. 1AD). As the polyp responded by producing the cone, the hypha continued to penetrate along the axis of the defense structure (Fig. 1). The polyp combated the continued penetration of the hypha by accreting subsequent layers of repair aragonite. In superficial regions of the colonies examined, where live coral tissue had been actively accreting skeletal carbonate immediately prior to collection, nearly every cone remained sealed (Fig. 2C). Only four of the cones observed in superficial corallites were perforated at their vertices (Fig. 2D), marking a possible successful breach of a corallite during the residence of its polyp. At present, the effect of the invading hypha on the penetrated coral tissue is unknown.

Hyphae of the endolithic fungi were observed to run just below the skeletal surface and to branch frequently, with branches directed toward the surface of the corallum (Fig.3). Diameters of boring tunnels left in the skeleton by endolithic fungi, including those tunnels observed within cones, fell well within the range of those reported from P. lobata (Table 1).

In addition to attempting to penetrate occupied corallites, endolithic fungi were observed to attack filaments of the endolithic alga O. quekettii (Fig. 4), which was present in all corals under study. Haustorial attachments of fungal hyphae to algal filaments were also similar to those observed in Porites lutea and P. lobata (7, 13). However, since we could not determine whether the filaments of O. quekettii were alive at the time of fungal attachment, the nature of this relationship (i.e., saprophytic or parasitic) could not be resolved.

In fractured samples of M. cf. studeri, a macroscopically visible green band was observed extending parallel to the basal plate about 2 cm below the growing coral surface. Examination of scanning electron micrographs of resin-cast preparations revealed that the green band contained both algal and fungal filaments (Fig. 5). Some of the filaments in the lower part of the green band exited the corallum and spanned pore spaces. These filaments, which inhabited internal spaces in the corallum, were calcified (cf. 15) (Fig. 6). They should be described as cryptoendolithic rather than euendolithic, the latter referring only to filaments that penetrate through the carbonate of the corallum (cf. 16) (Fig, 5). No internal green banding and no cryptoendolithic filaments were detected in the other corals under study. The absence of green banding in skeletons of the faster growing species examined, despite the confirmed presence of endolithic algae, is consistent with the proposed mechanism of band formation, which predi cts that green bands form during periods of reduced skeletal accretion rates (8).

The results presented here establish that the relationship between hermatypic corals and endolithic fungi, previously documented for P. lobata (7, 13), also occurs in corals with rapid axial growth. In addition, we extend evidence of this phenomenon to a second and third family of important reef-building corals, the Acroporidae and the Pocilloporidae. Lastly, we extend farther the already widespread geographical documentation of this phenomenon from Moorea, French Polynesia (17[degrees]30'S; 149[degrees]50'W) (7), and Mayotte, Comoros Archipelago (44[degrees]27'N; 1[degrees]8'W) (13), to our study site at Johnston Atoll (16[degrees]44'N; 169[degrees]32'W), recognized as one of the most isolated coral reef habitats in the world (17).

Similar published observations suggest the possible ubiquity and circumtropical distribution of this phenomenon. For example, Constantz (18, figs 2e, f) depicted structures (which the author referred to as "skeletal granulations") in Diploria labrynthiformis, a West Indian faviid coral, that were nearly identical in size and shape to cones described from P. lobata (7) and observed in our study. Lukas (10) reported endolithic fungi to be present in 10 out of 12 species of Atlantic and Caribbean corals examined, spanning 8 genera. Scherer (19) recorded conical structures, somewhat larger but similar in shape, in Colpophyllia and Montastrea, and attributed them to endolithic algae (19). Sato (20) described cone formation by polyps in response to attempted algal penetration into occupied corallites, thus providing an independent account-of the same phenomenon. The diameters of penetrating filaments described in both Scherer (19) and Sato (20) are significantly larger than the diameters of the fungal hyphae we o bserved, and correspond closely to the ranges reported for O. quekettii. The response of the polyps, however, is similar in that layers of compact, fine crystalline repair carbonate are deposited at points of attempted endolith penetration.

The nature of the defense response exhibited by corals in response to chronic interactions with endolithic fungi, and perhaps to less frequent interactions with endolithic algae, suggests a dependence on their ability to rapidly deposit [CaCO.sub.3] at sites of attempted endolith penetration. Thus, factors that directly or indirectly impair skeletogenesis in corals--such as elevated sea surface temperature (21), coastal eutrophication (22), and increased atmospheric [CO.sub.2] (23)--could compromise the ability of corals to defend themselves against endolithic fungal attack. Seasonal fluctuations in environmental variables that affect skeletal growth, such as the intensity of photosynthetically active radiation (PAR) or of UV-B (24), may also affect the relative frequency of coral-fungal interactions. Thus, a coral's inability to deposit sufficient repair aragonite, in conjunction with factors that may increase the frequency of coral-fungal interactions, could increase the regularity with which hyphae are su ccessful in breaching the skeletal surface of actively growing corallites (Fig. 2D). This is likely to be deleterious to the host coral's health.

Intensified defense activity of corals against endolithic fungi may, in turn, compromise a coral's ability to defend itself against other pathogens such as bacteria (25) or to invest energy in other processes, such as tissue regeneration, that maintain the integrity of the colony (26). The ability of corals to recover following bleaching events may also be weakened by their active defense against chronic attack by endolithic fungi (see Figs. 1 and 2).

Much attention has been drawn to emerging epizootics as threats to the welfare of coral reefs (27, 28). The conclusions from the present study indicate that reef corals exist in precarious dynamic equilibria involving all four symbiotic partners. Morbidity could, therefore, result from a disturbance in this equilibrium in which either endolithic fungi become successful opportunistic pathogens or the increased frequency of fungal attacks compromises the host sufficiently to succumb to additional pathogens. Thus, a shift in this balance, involving active defense against chronic host-fungal interactions within reef-building corals, may render endolithic fungi a previously unrecognized threat to coral reef ecosystems worldwide.

Acknowledgments

We thank Steven Oliver and Spence Smith for collecting samples, and Dr. Phillip Lobel for his support. We also thank the Boston University Earth Sciences Department, specifically Dr. Joel Sparks, for granting us access to their facilities. Funding was provided by a grant from the U.S. Army Research Office (# DAAG55-98-1-0304) for the Johnston Atoll Ocean and Reef Ecosystem Study.

(*.) To whom correspondence should be addressed. E-mail: cbentis @bu.edu

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                   Dimensions of microbial endoliths and
                   conical defense structure: all units
                   are in micrometers ([mu]m); values in
                    parentheses represent the standard
                    deviation and are followed by the
                        number of observations (n)
Measurement            Acropora Cytherea         Acropora humulis
Cone height         6.71 ([pm]0.31), n = 76  11.22 ([pm]4.09), n = 16
Cone width         12.73 ([pm]0.48), n = 76 18.14 ([pm]4.10), n = 16
Max/min cone height        17.82/2.32               21.81/6.60
Max/min cone width         30.08/7.4               20.67/12.35
Fungal diameter     1.43 ([pm]0.53), n = 80  1.52 ([pm]0.28), n = 61
Max/min fungal
  diameter                 4.12/0.32                 2.36/.7
Algal diameter       3.86([pm]1.0), n = 12   10.84 ([pm]2.95), n = 10
Max/min algal
  diameter                 5.76/2.67                14.35/4.32
Measurement          Montipora cf. studeri       Porites eydouxi
Cone height         15.47 ([pm]3.16), n = 6 27.01 ([pm]10.81), n = 59
Cone width         19.07 ([pm]2.80), n = 6 13.88 ([pm]2.69), n = 59
Max/min cone height        29.63/7.4               59.98/9.57
Max/min cone width        29.39/2.41               22.38/10.18
Fungal diameter     1.32 ([pm]0.30), n = 21  1.20 ([pm]0.20), n = 25
Max/min fungal
  diameter                 1.68/.39                 1.66/.77
Algal diameter      4.25 ([pm]0.80), n = 80  4.59 ([pm]1.08), n = 25
Max/min algal
  diameter                 5.91/2.72                 7.00/2.83
Measurement            Porites lobata [*]
Cone height         10.73 ([pm]3.28), n = 26
Cone width         10.80 ([pm]2.0), n = 55
Max/min cone height        20/no data
Max/min cone width         20.07/7.0
Fungal diameter     1.48 ([pm]0.27), n = 49
Max/min fungal
  diameter                   2.5/1
Algal diameter      5.93 ([pm]1.28), n = 37
Max/min algal
  diameter                   3.5/10
(*.)Data for P. lobata from reference 7.
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Author:BENTIS, CHRISTOPHER J.; KAUFMAN, LES; GOLUBIC, STJEPKO
Publication:The Biological Bulletin
Date:Apr 1, 2000
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