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Home , Agaricia, Astrocoeniidae, Black band disease, Colpophyllia, Eusmilia, Folliculinidae

DISEASES OF AQUATIC ORGANISMS Vol. 69: 75–78, 2006 Published March 23 Dis Aquat Org

Folliculinid : a new threat to ?

Aldo Cróquer1,*, Carolina Bastidas1, Diana Lipscomb2

1Departamento de Biología de Organismos, Universidad Simón Bolívar, 1080-A, 2Department of Biological Sciences, George Washington University, Washington, DC 20052, USA

ABSTRACT: This is the first report of a putative pathogenic protozoan that has been associated with Caribbean corals. Previously, only 2 of the phylum Ciliophora had been linked to diseases, and they were exclusive to the Indo-Pacific region. In this study, a ciliate of the Halo- folliculina was found on 10 hard coral species at the National Parks of Los Roques and Morrocoy, Venezuela. The general morphology of this ciliate is very similar to that of Halofolliculina corallasia from the Indo-Pacific, which is known to cause skeletal eroding band. None of the other 31 genera in the family Folliculinidae are known to cause diseases in corals or in any other species. The presence of this ciliate, which shows a prevalence comparable to that of other epizootics in the Caribbean, suggests it could be a new threat to the coral reefs of this region.

KEY WORDS: Coral · Ciliate · Disease · Caribbean · Coral reefs

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INTRODUCTION Many parasitic and pathogenic species of are known for their ability to cause massive mortalities in Coral diseases have been reported world-wide, marine invertebrates (Harvell et al. 1999, Gómez-Gutier- across oceans and bioregion provinces (Harvell et al. rez et al. 2002). In comparison with other protozoan 1999). Nonetheless, most coral diseases show a nar- phyla, the phylum Ciliophora contains only a few para- row distribution and occur within specific geographic sitic species (described in Antonius & Lipscomb 2001). regions only. For instance, the yellow band syn- Only 2 (SEB and BrB) out of the 18 coral syndromes drome, white plague type II and dark spots are which have so far been described (Sutherland et al. restricted to the Caribbean (Weil 2004), while other 2004), have been associated with the presence of the syndromes such as pink spots, porites ulcerative ciliates Halofolliculina corallasia (Antonius 1999, Willis white spot disease, bacterial bleaching, brown band et al. 2004) and Helicostoma nonatum (Borneman (BrB) and skeletal eroding band (SEB) have only 2001), respectively. Both ciliates have been considered been reported for the Indo-Pacific (Willis et al. 2004) exclusive to the Indo-Pacific corals, although H. coralla- and the (Winkler et al. 2004). Even the sia has been specifically searched for in the Caribbean few syndromes that are common to different biore- (Antonius & Lipscomb 2001). No other species of the gions appear to have a different etiology. For exam- genus Halofolliculina, and none of the other 31 genera in ple, molecular investigations showed differences in the family Folliculinidae, are known to cause diseases in the bacterial consortium associated with black band corals or in any other animal. The distribution of H. coral- disease (BBD) between bioregions (Frias-Lopez et al. lasia within Indo-Pacific reefs remains elusive because 2003). Differences and similarities in the ecology and qualitative surveys have been performed in the northern etiology of coral diseases among bioregions (GBR), the Mauritius islands and remain relatively unexplored, probably due to the the Sinai Peninsula only (Willis et al. 2004). In this study, fact that research started only 3 decades ago when we report for the first time a folliculinid ciliate of the Antonius (1973) was the first to describe a syndrome genus Halofolliculina sp. associated with 10 hard coral affecting corals. species from the Caribbean.

*Email: [email protected] © Inter-Research 2006 · www.int-res.com 76 Dis Aquat Org 69: 75–78, 2006

MATERIALS AND METHODS RESULTS

In April 2004, we first observed a folliculinid ciliate The general morphology of the Caribbean ciliate is on the hard coral fastigiata (see Veron very similar to that of Halofolliculina corallasia from 2000 for an authoritative work on coral species) in the Indo-Pacific (Fig. 2A). Both H. corallasia and the the coastal National Park of Morrocoy, Venezuela Caribbean form are sessile in a with the cell (Fig. 1A). This finding prompted us to survey a body attached at its pointed posterior end. The lorica is month later the reefs of Dos Mosquises Sur at the sac-like with a rounded posterior, and a cylindrical National Park of Los Roques, an oceanic archipelago neck that angles up from the surface at about 45°, located 160 km north of the Venezuelan mainland with a single sculpture line circumscribing it. The cell (Fig. 1B). In Los Roques 3 reef habitats were sur- is elongate with 2 conspicuous peristomial wings veyed: a shallow barrier reef (2 to 3 m depth) and a (Fig. 2A) bearing feeding cilia. Upon cell division shallow and a deep (8 to 12 m depth) . (asexual reproduction), vermiform, migratory larval The barrier reef is more exposed to waves than the stages are produced (Fig. 2B). Also, the sessile forms fringing reef, and the two are 1 km apart (Fig. 1C). seemed able to abandon their lorica and actively seek On the barrier reef 2 zones were clearly distin- suitable substrata (Fig. 2C). were distin- guished; one dominated by palmata and guishable in large numbers inside the ciliates (Fig. 2C), the other by Acropora cervicornis. In the former suggesting that ciliates might ingest the zooxanthellae. zone, colonies were examined along 5 belt transects However, further examination is required to determine of 25 × 2 m each, by carefully checking with magni- whether they are able to establish a with the fying lenses to verify the presence or absence of cili- , as other protozoans do (Lobban et al. 2002). ates. In the zone dominated by A. cervicornis, we We are preparing a detailed anatomical description evaluated 20 quadrats of 0.25 m2. The quadrats were of the Caribbean folliculinid Halofolliculina sp. to be spaced 5 m apart, which allowed for evaluation of at published in a forthcoming article. least 7 physically separate thickets of A. cervicornis. Halofolliculina sp. was obse rved on Eusmilia fasti- Within each quadrat we counted the number of giata () at Morrocoy, and on the follow- branches (defined as uninterrupted living tissue), and ing 9 hard coral species at Los Roques: Acropora checked them for ciliates. The number of branches palmata, A. cervicornis, A. prolifera (Acroporidae), per quadrat ranged from 5 to 27. Five quadrats had Colpophyllia natans, annularis, M. faveo- <25% cover, 8 had 25 to 50% cover, and 7 had 50 to lata, M. franksi, labyrinthiformis (Favi- 75% cover of A. cervicornis. idae), and Madracis mirabilis (Astrocoeniidae). Coral In the shallow fringing reef we evaluated 3 belt colonies affected by the ciliates had a dark band that transects following the procedure described above for separated healthy and dead or bleached tissue the Acrapora palmata zone. In the deep fringing reef, we searched for ciliates in coral colonies intercepting each of the three 25 m long transects. The prevalence of the ciliate was estimated as the ratio of the number of affected patches or colonies to the total number of patches or colonies in- spected within the observed unit. In addition, for each patch of A. cervi- cornis prevalence was estimated as the number of branches with ciliates divided by the total number of branches. Live coral samples were taken to the laboratory where the ciliates were ex- amined using a stereo and compound microscope. All coral samples with cil- iates remained in Bouin’s fixative for Fig. 1 (A) Cayo Sombrero (1) in the Morrocoy National Park (a on map inset); 48 h, were washed with tap water and (B) Dos Mosquises Sur (s) in the Archipelago of Los Roques National Park (b on finally stored in 70% ethanol for map inset), scale bar = 15 km; (C) closer view of Dos Mosquises Sur further microscopic examination. showing the barrier reef (2) and the fringing reef (3), scale bar = 1 km Cróquer et al.: Folliculinid ciliates in the Caribbean 77

Fig. 2. Halofolliculina on Acropora palmata, Colpophyllia natans and A. cervicornis. (A) General aspect of the ciliate (×50). (B) Young, free-swimming larval stage of the folliculinid (length 78 µm). (C) Presumptive adult, elongated, free-swimming stage outside of the lorica; zooxanthellae visible inside the protozoan (×200). (D) Ciliates on A. palmata; live and dead tissue to the left and right of the band, respectively (×12). (E) Ciliate in low density on C. natans (×18). (F) A. cervicornis with ciliate clusters resembling

(Fig. 2D). Upon close examination in the field, the dark patches of A. cervicornis (10%), and its prevalence per band consisted of small black dots (ciliates) that are branch was 0.5%. In addition, at this site, the ciliate easily discerned with magnifying lenses. At Los had an overall prevalence of 1.2% among 1266 Roques, the most affected species, in terms of the colonies belonging to 11 hard coral species. As only density of the ciliates and their prevalence among acroporids were affected here, the prevalence reached colonies, were acroporids. In the barrier (wave- 11% in 101 colonies of A. palmata, whereas 2 out of 11 exposed site), 85% of the patches of A. cervicornis had colonies of A. cervicornis and 2 out of 2 colonies of A. at least 1 branch affected by ciliates. For this coral prolifera were also affected. Similarly, in the shallow species, the prevalence among branches within a fringing site, the ciliate had a prevalence of 2.6% patch ranged from 0 to 40% (up to 7 branches affected among 513 colonies of 12 hard coral species. A. in a 0.25 m2 area), with a mean of 18% of the branches palmata was the only affected species here, and the affected by the ciliate among all patches. In contrast, prevalence of the ciliate was 10.5% among 133 co- appeared in only 2 out of the 20 lonies. Thus, at the 2 shallow sites, barrier and fringing 78 Dis Aquat Org 69: 75–78, 2006

reefs, A. palmata showed a similar prevalence of the corals in the region, as it is possible that the ciliate only ciliate. recently invaded the Caribbean from the Indo-Pacific. In the deep fringing reef, which had a mean hard This is a plausible hypothesis in view of the high rates coral cover of 57%, the prevalence of the ciliate was of dispersion of marine parasites (McCallum et al. 2003) 9% among 91 colonies comprising 13 coral species. and the numerous damaging invasions that have oc- The ciliates were observed on 1 colony of Colpophyllia curred among marine ecosystems (Ruiz et al. 2000). natans, 3 colonies of Montastraea annularis, and 4 In conclusion, the high prevalence of this folliculinid colonies of M. faveolata. These coral species had a and its capability to infect a large number of Caribbean cover of 18, 8 and 24%, respectively. Ciliates were also coral species show that these ciliates are no longer observed outside sampling units in Madracis mirabilis restricted to the Indo-Pacific, but affect corals on a and Diploria labyrynthiformis. We did not detect cili- global basis. ates in any of the following species observed within the sampling units: Montastraea cavernosa, Acknowledgements. We thank D. Bone for sharing his labora- meandrites, Isophyllastrea rigida, Diploria strigosa, tory facilities, Fundación Científica Los Roques for allowing Porites astreoides, P. branneri, P. porites, Siderastrea the use of their facilities, L. M. Márquez, G. Smith, P. Zanders, siderea, agaricites and Favia fragum. and C. Bosque for their helpful comments on the manuscript, and 2 anonymous reviewers for additional comments.

DISCUSSION LITERATURE CITED

We provide the first report of a folliculinid ciliate Antonius A (1973) New observations on coral destruction in associated with corals in the Caribbean. This ciliate was reefs. Assoc Isl Mar Lab Caribb 10:3 found in Venezuela on 10 hard coral species, including Antonius A (1999) Halofolliculina corallasia, a new coral-killer most major reef builders. In a reef at Los Roques, the ciliate on Indo-Pacific reefs. Coral Reefs 18:300 Antonius A, Lipscomb D (2001) First Protozoan coral-killer prevalence of this ciliate was up to 85% among patches identified in the Indo-Pacific. Res Bull 481:1–21 of Acropora cervicornis, 11% among A. palmata Borneman EH (2001) Aquarium corals: selection, husbandry, colonies, and from 3 to 9% for 20 hard coral species and natural history. THF Publishing, Neptune City, NJ examined. The high prevalence among acroporids was Frias-Lopez J, Bonheyo GT, Qushend J, Fouke BW (2003) similar between a wave-exposed reef site and a rela- associated with black band disease in Caribbean and Indo-Pacific reefs. Appl Environ Microbiol tively less exposed shallow site. Ciliate densities appear 69:2409–2413 to be fairly variable within and among coral species. Gómez-Gutierrez J, Paterson WT, De Robertis A, Brodeur RD While some colonies had very few ciliates (Fig. 2E), (2002) Mass mortality of krill caused by parasitoid ciliates. making it difficult to attribute tissue mortality to them, Science 301:339 Harvell CD, Kim K, Burkholder JM, Colwell RR and 9 others other colonies showed clusters of ciliates in high densi- (1999) Emerging marine diseases — climate links and ties (Fig 2F). In colonies with high ciliate densities, it anthropogenic factors. Science 285:1505–1510 seems likely that ciliates infect coral tissues which have Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawloswki already been damaged by bleaching or predation, or J, Foissner W (2002) Ciliate– symbiosis affected by diseases such as white band disease. Fur- spotted on reefs. Coral Reefs 21:332 McCallum H, Harvell CD, Dobson A (2003) Rates of spread of ther research is necessary to determine the set of condi- marine pathogens. Ecol Lett 6:1062–1067 tions that affect ciliate density and the way this is asso- Ruiz GM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq ciated with damage to corals. A, Colwell RR (2000) Global spread of microorganisms by Despite its abundance in Los Roques, this ciliate had ships. Nature 408:49–50 Sutherland K, Porter JW, Torres C (2004) Disease and immu- previously remained unnoticed in the Caribbean, al- nity in zooxanthellate Caribbean corals. Mar Ecol Prog Ser though many scientists have worked on diseases, and 266:273–302 looked specifically for Halofolliculina corallasia Veron JEN (2000) Corals of the World. Australian Institute of (Sutherland et al. 2004). In particular, this ciliate was Marine Science and Cooperative Research Centre, not found in reefs of at least 3 Caribbean countries sur- Townsville Weil E (2004) diseases in the wider Caribbean. In: veyed between 1997 and 2000 (Antonius & Lipscomb Rosenberg E, Loya Y (eds) Coral health and disease. 2001). It is possible that this ciliate has remained un- Springer-Verlag, Berlin, p 35–67 noticed due to its superficial resemblance to BBD when Willis BL, Page CA, Dindsdale EA (2004) in the it occurs in high densities (Fig. 2F). Also, the relatively Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, p 69–104 low abundance of acroporids in most Caribbean reefs Winkler R, Antonius A, Renegar DA (2004) The skeleton as well as their susceptibility to other diseases may eroding band disease on coral reefs of Aqaba, Red Sea. have contributed to researchers overlooking this condi- PSZN I: Mar Ecol 25(2):129–144 tion. Alternatively, it may represent a new threat to the

Submitted: December 15, 2004; Accepted: May 16, 2005 Proofs received from author(s): January 22, 2006