Rev. Biol. Trop., 46 Supl. 5: 145-156, 1998
Epizoism: a new threat to coral healtb in Caribbean reefs
Arnfried Antonius1 andEnrie Ballesteros2 I ¡nst. Paleontology, Univ. Vienna, Althanstrasse 14, A-I090 Vienna, Austria. 2 Centre Estudis Avanr;ats-CSIC, C. Santa Bárbara sIn, E-17300 Blanes, Spain.
(Ree. 25-VII-1997. Rev. 26-IlI-1998. Aeep. 5-V-1998)
Abstract: Coral reefs around Carrie Bow Cay, Belize, Central America were investigated in 1972 and reefs of the 10hnPennekamp Coral ReefState Park offKeyLargo, Florida in 1973. Both sites were resurveyed in 1997 and a new threat to coral health was found: a rather epizootic occurrence of other organisms overgrowing living coral. On the reef-tlat of the Barrier Reef north of Carrie Bow Cay, there are fields of Aeropora eervieornis and Porites porites, scattered over shallow sand-bottom. A large number of these corals show either "tufts" of blue-green algae, or fila mentous "tlags". Bothmay coversubstantial portions of individual coralla; theliving tissue disappeared at the of con tact area. Another type of overgrowth on living corals is represented by the red alga Metapeyssonnelia eora/lepida, as well as the brown alga Lobophora variegata. Bothovergrow mainly Millepora eomplanata and M alcicornis, but a1so other corals withsmooth surface, sueh as Porites porites and P. astreoides. This syndrome occurs about equally abundantaround CarrieBow Cay, Belize, andin reefs offKey Largo, Florida. A similar kind oftightly attached over growth is represented by the sponge Cliona earibbea. It was found regularly in the reefs aroundCarrie Bow Cay on a wide variety of coral species. An identical type of epizoism is represented by Chondrilla ef nucula, which, so fa r, was observed only in Belize. Al! these new syndromes together amount to a considerable coral-degrading factor, which was not found in thesereef s 25 years ago.
Key words: Reef corals, space competitors, epizoism, coraldeath, reef degradation.
Coral reefs around CarneBow Cay, Belize, When both reef-sites were resurveyed m Central America, located at 16° 48' N, 88° 05' early 1997, the most striking differences in W (Fig.l) were investigated in 1972, and reefs comparison to the old surveys were that : 1) of the JoOO Pennekamp Coral Reef State Park much larger portions of reef-crest and back off Key Largo, Florida, located at 25° 07' N, reef areas aredead today, and2) a qualitatively 80° 18' W (Fig.2) in 1973 (Antonius 1974). new threatto coral healthhas emerged, consist Since 1972 was the year of discovery of the ing of a rather epizootic occurrence of certain black-band disease (BBD) of reef corals Cyanophyta, Rhodophyta, Phaeophyta, and (Antonius 1973), special emphasis in both sur Porifera overgrowing living corals. Thus, sub veys was put on coral health.Thus, along cer ject of this paper is a qualitative description of tain transects, Uve, diseased, otherwise impact newly observed phenomena of epizoism ed, anddead corals were recorded. Impacts on degrading coral health. Uve corals otherthan diseases was found to be This does not mean thatthe "old" maladies mainly feeding damage by the fireworm have disappeared. On the contrary, BBD and Hermodice carunculata (Antonius 1973, 1975) white-band disease (WBD)are still common at inthese oid surveys. both locations (Antonius 1981), coral-tissue- 146 REVISTA DE BIOLOGIA TROPICAL
t N
16°50' ,') (,.: Victoria � �
I Carrie Bow Cay 1:) I • ./ 1j' \ Channel 5km 88°10'
Fig. 1. To the left( = west) the mainland of Belize just south of the town of Dangriga with the mouth of the SitteeRiver. To the right (= east) the patch-reef system ofthelagoon andthe barrier reefwith Tobaceo Reef in the north, Curlew Bank in the south and Carrie Bow Cay in the center.
;¡� " , ' --.....,/ / "
shelf edge,/ ) \ /.�: . t Hawk 25°07' N ,,l" Greci D�Rocks ROCks JI �f ,,/ � : ', ' � � //
Fig. 2. To the left (= west) Key Largo withLargo Sound (L. S.) andSouth Sound Creek (S). To the right (= east) theWhite Banks area withthe Key LargoDry Rocks and Grecian Rocks reefs. The shelf edge marks the30m isobath.
bleaching (TBL) is rampant especialIy in MATERIALS AND METHODS Belize (Antonius, in prep.), while Florida is beinginvaded by an array ofpreviously little or Underwater, on-site observations were unknown syndromes, such as white-pox, yel made along a total of twelve transects: 3 north low-blotch, white-plague (Goreau et al. 1998), and 3 south ofCarrieBow Cay, Belize, as well white-plague type II (Richardson et al. 1998), as 3 transects on Key Largo Dry Rocks and 3 or rapid-wasting disease (Cervino et al. 1997). on Grecian Rocks, Florida. However, in our opinion, the combined phe The Belt Method was used throughout in nomena of epizoism, described in thispaper, order to register all syndrom,?s on corals in the may pose an even more severe threat to coral transectsas indicators ofthe healthcondition of health and wellbeing of the entire reef ecosys the respective reefs (Antonius 1995a). It is a temo semi-quantitative time-count technique that uses 30-min scans to quantify frequency of occurrence of coral diseases and other coral- ANTONIOS & BALLE�TEcROS:A new threatto coral health 147
degrading syndromeson � .scale from zerQto ingdataonthechanges tll.at bay�t�en place in six. H(}wever, forthepmp()se ofthis paper,per� these reefs overtime, will be fOtthcoming at a centages. of afllicted· specimens. of the respec� future date (Antonius, inprep.): tive corakspecies·were calculated. Anover�n The second point Usted in theIl1tr0duction, accountofcoral (andfuusreef) heal tb, dealing.. the new phenom�na ofothergrgatírsms over withallthepresentIy.knowl'l syndromes onreef growing living coral, is· the �lÍbject of this corals (Antonius 19951:», will be published papero We wOllld like topoint óut thatthe des elsewhere (Antonius, in prep,). ignation as " new'Lphenornena shaU notsuggest Samplestákenlli théfieldwerepreserved m · that these sylldroni�s 1Íadnot exist�ed in· the 4% formalin-seawater,·as well as in 70% dena past, but mere]y that fuey had not been a threat tured ethanol. AH· voucher specimens \Vere to coral· and to coral reef health a few decades deposited in the Herbario del Centre d'Estudis ago. Avancats, CSIC, in Blanes, Spain. Therespec� tive access'ion-numbers are listed in the Blue-greeo algae: The Atlaritic Barrier "ResuIts" north 9fCarrie Bovv Cay, section. .Reefimrnediately . . . ··, Belize,consists ?fan approximatel)i 50m-wide . reefcrest,madeuPrnainly of Acroporapalma MSULTS ta··and Millepora cdmplanata, foUowed by a
Fot somebod \Vlio ha� nó!1:>eenhackto· � . TABL�J· th�se reefs for 25 years, fue· frrst sight· was a · f!�al·sh()ck. E�pecially the reefs around Carne Sum.mary ofpercentages ofcoral populations Bow Cay, �in Belize which wereteeming with óvergrownbjJeitherc)'a�dphytes, or ftlacroal grouper,snapper, trlggerfish,other colorfulreef gae, or sponges inreeftofCarrie Bow Cay, . Belize and Kéy Largo, Floridq. (n.r. = notreg fish, andwith Iobstenmdconchint�e oId d�ys, ister�d) ··· �e now ghostlt empty. Tlie onlylargerfish · s:endurin�onelllo�th �fsurveywas onepai� rotfisb andnyO 'b a.rracudas. I:'i�hpo pulations in��d�theiNatioriaIM aripe S�chlary aí I(ey Largo, Floridao�appearedfobe···in . ·· é M,acroalgae Florida d�ad todaY;·And this is trUe for Carrie B0� .· cBelii . % .gr6wingori '. %. ,., Reefingoo�co#ditio1l25in. BeHze, aswell as fór Grecian".Rock§ . and Key Largo Dry.. �ocksin Fig. 3.The typicaJ"tufts" of Oscillatoriasubmembranacea on branchesof Porites porites. One ofthe branches hasbeen com pletely covered by the cyanophyte. roughly 200m-wide reef flat that is about 1m swept in from the outer reef, getting caught in deep behind the reef crest and2m deep toward the branches, is not known at presento the lagoon (Rützler and Macintyre 1982). Right Followíng Drouet's taxonomy, we identi behind the reef crest, the bottom is mostly rub fied the "tufts" as Oscillatoria submem ble inbetween numerous Montastrea annularis branacea and the "flags" as Schizothrix mexi and Porttes astreoides heads. Towards the cana, while according to classic taxonomy the lagoon, the floor becomes a sand-flat, studded "tufts" also match the characteristics of withAcropora cervicornis and Porites porites Microcoleus Iyngbyaceus, andthe "flags" those colonies. of Oscillatoria margaritifera. Since the taxon As mentioned earlier, compared to 1972, omy of blue-greens is notoriously difficult, def the 1997 survey showed a much larger percent inite identification will undoubtedly require age of still standing, but dead coral colonies. further investigation. This was the case on the reef crest as well as on Absolutely unequívocal, however, are the !he reef flat. A substantial part of this coral effects of this kind of overgrowth on the living mortality could be traced to cyanophytic over coral. There seems to be a positive correlation growth. About 50% of all A. cervicornis andP. between the size of the area of contact between porites colonies (Table 1) scattered over the alga and coral, andthe degree of degradation of reef flat show either"tufts" ofblue-green algae coral tissue: withincreasing size of thearea, the (Fig. J) or filamentous "flags" (Fig. 4) waving results of this contact become increasingly in the current. Both may cover substantial por severe. The coral tissue is usually found tions of these branching corals. Whether these bleached when thearea of contact is as small as cyanophytes had grown on the coral branches a few square-millimeters; when the alga covers from minute germs, or whether they were several square-centimeters, the coral tissue is ANTONlUS & BALLESTEROS: A new threat to coral health 149 Fig. 4. Waving "flags» of Schizothrix mexicana on branch-tips of Acropora cervicornis. Coral tissue is being killed by the cyanophytic cover. mostIy encountered in the process of dying; corallepida is under way, since it is a new once cyanophytic overgrowth occupies areasin species. Both algae overgrow mainly Millepora the order of magnitude of square-decimeters, complanata (Fig. 5) and Millepora alcicornis the coral tissue has, in most cases, died offand from the bottom upwards, but also other corals is completely gone. with smooth surface, such as Porites porites This particular problem of cyanophytes (Fig. 6) and Porites astreoides. This syndrome invading coral populations was, in February occurs about equally abundant around Carne 1997, encountered only to a minimaldegree in Bow Cay, Belize, and in the reefs off Key Florida. However, blue-green algae can be - Largo, Florida with percentages of afflicted and have been - a problem in Key Largo reefs individuals of these species ranging from 2 to (Table 1) and will be dealt with again in the 10 % (Table 1). "Discussion" . Both algae, Metapeyssonnelia corallepida Samples of Oscillatoria submembranacea as well as Lobophora variegata form a tightly aredeposited as EB-CBC-12 and EB-CBC-B, attached "skin" on the coral surface, with no while Schizothrix mecicana is represented by trace of living coral tissue left below thealgal EB-CBC-14. cover. In the field, the two species arehard to distinguish, sínce both are very darkwith razor Macroalgae: Another type of overgrowth sharp edge. In comparison, however, M on living corals is represented by the red alga corallepida appears even darker than L. varie Metapeyssonnelia corallepida, and the brown gata, with a violet hue and showing rather alga Lobophora variegata. While species deter straight edges, while L. variegata is tinted dark mination of L. variegata did not pose any prob olive with more rounded edges. Both algae start lem, systematic evaluation of Metapeyssonnelia to grow at the base of coral colonies which are 150 REVISTA DE BIOLOGIA TROPICAL Fig. 5. The rhodophyteMetapeyssonnelia corallepidagrowing over Millepora complanata. The edge ofthe alga is relatively straightand its color is a dark purple. Fig. 6. The phaeophyteLobophora variegata overgrowing sorne fingers of Pori/es porites. The edges of thealga areusuall y rounded andits color is a dark, drab olive-green. ANTONIUS & BALLESTEROS: A new threatto coral health 15 1 Fig. 7. The hadrorneridsponge Cliona caribbea growing on a largeDiploria labyrinthiformis. It probablystarted out at sorne spot of denuded coral skeleton, but proceeds to overgrowliving coral surfare. "dead", void of coral tissue and thus defense This does not mean, however, that less. From there they proceed upwards, now Metapeyssonnelia corallepida could not be overgrowing and destroying polyps and lethal for M complanata. Many cases have coenosarc. been registered of large frrecoraIs totally over Lacking observation time, the speed of the grown by fue rhodophyte. Thus, these colonies process is not yeí known, but the impact is evi stiH perfectly exhibit the shape and growth dent. Although coralpolyps appearundisturbed form of M complanata, but they are now pur irnmediately in front of the advancing alga, plish-black instead of the typical Uve yeUow. there is no trace of coral tissue left below the The same is true for L. variegata overgrowing tightly attached algaI cover. In fact, even the P. porites : colonies of this coral showing fm surface structure of the coral skeleton appears gers which areolive-black instead of thenormal to be eroded. Quite in contrast to ofuer syn Uve, bright greenish-grey, have been killed and dromes, M corallepida andL. variegata over overgrown by the phaeophyte. growingand thus killing offliving coral tissue, Samples are deposited under the numbers do not appearto open up theway for othercoral EB-CBC-7 and 11, as well as EB-KLF-l bioerosion, such as boring organisms. through6. However, in sorneinstances these overgrow ing macroalgaeseem to triggerWBD (Antonius Sponges: A similarkind of tightly attached 1995b). Thiswas definitely observed in cases of overgrowth, also starting at the base of fue Lobophora variegata overgrowing Porites coral colony is represented by the hadromerid porites andis suspected - but could not be veri sponge Cliona caribbea. Itwas foundregularly fied beyond a reasonable doubt - in cases of in reefs around Carne Bow Cay on Acropora Metapeyssonnelia corallepida overgrowing pa/mata (Fig. 8), Millepora complanata, Milleporacomplanata. 152 REVISTADE BIOLOGIA TROPICAL Fig. 8. Close-up of Ihe advancing front of Cliona caribbea on an Acropora palmata. The sponge not only kiUs offtite coral polyps, but a1so penetrates tite uppermostlayer of titeskeleton. Montastrea annularis, Diploria strigosa, Of the substantial A. palmata and M com Diploria labyrinthiformis (Fig. 7), Agarieia planala populations south of Carrie Bow Cay, tenuifolia, and relatively frequently on an estimated 5% of all colonies may be afflict Dendrogyra eylindrus, but only very rarely on ed, while not more than 1-2% of the other coral Aeropora pa/mata and Millepora eomplanata species are overgrown by C. caribbea (Table in Florida (Table 1). 1). The strikingexception is D. cylindrus which However, Cliona earibbea covering Uve is not a frequent species around Carrie Bow corals may be the second stage of the invasion. Cay, but under heavy attack by C. caribbea The sponge readily grows on dead coral sur (Table 1). Interestingly, this syndrome seems to ,faces, often enough wifu no living coral any be much less of a problem in Florida where where near. From fuese foofuolds it proceeds to only very few cases were observed on A. overgrow Hve portions of the coral colony (Fig. palmata and M eomplanata (Table 1). 7). In doing so, C. caribbea not only eliminates Another sponge, Chondrilla ef nueula, the coral's polypsand coenosarc, but also erodes apparently is behaving the same way. It starts theskeletal surfacestrucrure and even penetrates out at sorne dead spot of a coral colony, but the uppennost 1-2 cm of fue coral skeleton. proceeds from there to overgrow living coral However, just as was observed in fue case of surface. At present it does not seem to be a overgrowingmacroalgae, coral polyps appearto threat to reef health though, since only three be undísturbed immediately in front of the lead cases were found in Carrie Bow Reef, and ing edge of fuesponge. Thespeed of advance of none, so far, in Florida. One of these, however, C. earibbea is not yet known, but theposition of had almost completely enveloped a large several of fueseleading edges have been marked colony of Diploria strigosa (Fig. 9). in fuefield and will yield results in the future. 154 REVISTA DE BIOLOGIA TROPICAL almost haIf-a-meter in height and covering Millepora colonies inside ca field of living, large patches, killing offnot only stony comIs, bright yeUow ones. but also the very frequent sea-fans (1 Halas What both algae seem to have in common is pers. comm.). Thus,the reef is locally known as the faet that they can trigger WBD, a phenome the "algae reef' since then,and the cyanophyte non previously only observed to be linked with was tentatively identified as Lyngbya sp. eyanophytes (Antonius 1987, 1988). Throughthis Today, most of thestony corals are dead, and so mechanism L. variegata as well as M corallepi is the dense population of Gorgonía ventalina damay amount to ca force much more destru.ctive (Table 1). The large skeletons are still there, than any of them would be on their own. waving in the surge, while a new generation of Among coral-overgrowing and eoral-killing now hand-sized fans has begun tú grow. sponges, the most notorious to date is probably At Carrie Bow Reef in Belize, which is far Terpios sp. (Bryan 1973, Plucer-Rosario 1987 away from sources of man-made pollution, we and Antonius 1991b), or Tapias hashinota suspect that the problem is related to a decline respeetively (Antonius 1993, Rützler & Muzik in Caribbean water quality in general. Where 1993). T hoshinota which can infest hundreds should cyanophyte-promoting water-conditions of meters of coral reef in Micronesia (Bryan come from, if not from the open Caribbean 1973), has also been reported fromthe northem Sea? After aH, northeasterly trade-winds pre Pacífic, from Samoa to Taiwan(Plucer-Rosario vail in Belize during 70% of the year (Rützler 1987), from southem Japan (Rützler & Muzik & Ferraris1982). 1993), as well as from Mauritius (Antonius Of fue array of coral-overgrowlllg organ 1993) and Sinai. (Antonius 1996). Buí it was the brown alga Lobophora variegata is neve!" observed in Atlantic waters. oue previously observed by the However, there seems to exisí a true COUll authors tú damage comls. During terpart in the Caribbean. Cliona caribbea tions of coral health in Mauritius, mentioned tumed out tú amount to a majo!" coral-killing earlier, L. variegaía was observed to overgrow agent in reefs around Carry Bow Cay, Belize, siTIal! of Porites sp., Favia stellig and also occurring in Florida. Clíona species, era., ¡¡ud others (Antonius 199Ab, 1995b, such as C. caribbea, C. lampa, and C. varians Ballesteros, in However, even in the par have been observed as successtul competitors ver)' sick ,coral populatiol1s of Mauritius fol' space befare 1978). However, in press), the oue C. "n,fU""O_,O'N,,,¡,.,,n.,,",, (LOB) was not enCOUI1- among the Porites of the back··reef area, LOE arhounts to a factor. "lil1hHe LOE seems to be less of a threat in of different evrai another the mther indís:criminate manne!". rhodophyte Metapeyssonnelia As mentioned the sponge does not dcminant there. In this red prey 011 ana probably can not even setde m true cYanobacteriosponge is por p:írte de diversos organismos bentónicos. Las poblacio- . Chondrilla sp. in Carrie'Bo'W Reef, w:hieh' ne,s de Acropora cervicorn¡sy Poritesporites situadas sobre los fondos arenosos someros de la plataforma arrecifal del could be C. nucula, describéd as coral-over norte de CarrieBow Cay estaban,�n p:írte,recubiertas por growing from Puerto Rico (Vincente 1990), but penachos o láminasde laS cianoficeas Oscillátoriasubmemc mightbe a neW species (K Rützler, pers. branl1cea y Schizotl¡rá mexic121l4. Aproximadamente el , con comm.). The Chpndrilla species found in 50% de los ,corales estaban afectados, destrucción del tejido vivo del' coral en las áreas de contacto con las ciano however, is a wholeorder ofmagnitude Belize, ficeas. Desconocemos sUas"cianofíeeas se desarrollaron die less frequentthan Cliqnacari!Jqeaand does no! re,ctamentesobrelos eoraJeso bien si se-engl!l1eharona ellos ' ,� , ' ACKNOWLEDGMENTS" ,,' .,:<,' , " ' " , . ' �ilpport. ofíthese. investigatiOtls by th,e Austriárl �'?ienóéI1(mnd�tion,(FWF)ian4 the Al1tbn1uS,A. 1973. New observations on eoral destruction ¡nreefs.�bs. �ssoc .Isl. Mar.Lab.. Carib.10: 3. '�miths01*ln Institution (for fieldwor� " in . BelIze) is grate,fullyacknowledged. Joint Ál)tónius;A 197;4. Finalreportofthe eoralr�efgroup of researeh by the co-autbors wasfacilitatedbya . the,Flol'í�áK�ys Project fortheprojectyear 1973. HarborBranéb Foun¡jatiQn, Fo!1Pierte, Florida., 20lp :frav�l grant ,from tbe bureau oí "Accionés Iutepradas,' HisparlO-Austríaeas". Cordial , per� AntonitlS,A, 1975. Predati()n bythe polychaete lferrnodice can¡ncul(jtao n reefcorals. InH.G:Multer (ed:). Field sona.l tha11ks go to K.,Rütz,ler audioJ Halasfor - , . gíliíle tasome carbonate rockenvironment$. Kendall invalllable assistanceinthe field. Húnt. pp.133}c',133M. AI1tonius, A. 198I. The "band" diseasesiri eoralreefs_ Pi'oc. Fourth Intemat. Coral Reef Symp., Univ. REsuMEN Pllilippmés,Manila 2: 7�14. Antonills,A. 1985, COral dis ases inthe .lndo-Pacific: A Los lliTe(lifes coralinos situados alrededor de Carrle � first record. p.S.Z.N.l: Mar. Eco\. 6: 197-218 . . Bow Cay, Belice (América Central), Y I()sarrecifes del JohnPeo/lekámp Coral Reef State Pªtk, en Key X.argo; Antonius"Á. 1987. Suivey ofRed Sea coralreefhealth. l. Florida, fi.¡eron exp10radl?sen 1972y 1973, respec�¡va 'eddahto Jizan. P�oe.8audi Bio!. 80c, 10: 149cl63 ,mente. En ambas prospecciones se pusoe�pecial atención al estado de 10scoralo;::S puesto queenl?'i2 senabía,descu Antoni�,/J.. ! 988. '9j�tril:)lltion and dynamicsof coral dis in th�eaSiem :Red Sea. Prc. 8iXíb Intemat. bíert(), la enfennedad de la bandánegra(BlackBand dis eases � J.C. 2: ease)que atao;:a a los corales. A.mboslugares fueron visita, Coral ¡{eefSflllP., Univ.,Towl1sviIle;Australia d()s nu!eyamo;mteen1997 o1>serváildosenuevos sintomasde 293-298. degtadaciónronsistentesen el recubrimiento de los coÍ'81e$ 156 REVISTA DE BIOLOGIATROPICAL Antonius, A. 1991 a. Etat de santé des coraux. In: J. Muller Cervino, J., T. J. Goreau, R. Hayes, G. Smith, D. Santavy, (ed.): Étude des ecosystemes littoraux de Maurice. E. C. Peters, K. Meyer, 1. Nagelkerken & B. Boekhout. ECC projet 946/89, rapport noA: 16-33. 1997. A new Caribbean coral disease. Abs. AMLC-97, Univ. Costa Rica. 43 p. Antonius, A. 1991b. La maladie des coraux dans les zones tests no. 1 et 2. In J. MuIler (ed.). Étude des ecosys Plucer-Rosario, G. 1987. The effect of substratum on the temes littoraux de Maurice. ECC projet 946/89, rap growth of Terpios, an encrusting sponge which kills port no. 5. pp:145-165. corals. Coral Reefs 5: 197-200. Antonius, A. 1993. Coral reef health in Mauritius. Abs. Richardson, L.L., M.w. Goldberg, R.G.Carlton & le. First Europ. Meet. J.S.R.S., Univ. Vienna, Austria: 2. Halas. 1998. Coral diseaSe outbreak in the Florida Keys: Plague Type II. Rev. Biol. Trop. 46:187-198. Antonius, A. 1995a. Coral diseases as indicators of reef health: Field methods. Proc. Seco Europ. Meet. Rützler, K. & J. D. Ferraris. 1982. Terrestrial environment l.S.R.S., Pub!. Servo Geo!. Lux. 29: 231-235. and climate, Carrie Bow Cay, Belize. pp:77-9J. In K. Rutzler & I. Macintyre (eds.). The Atlantic Barrier Antonius, A. 1995b. Pathologic syndromes on reef corals : Reef Ecosystem at Carrie Bow Cay, Belize, l. A review. Proc. Seco Europ. Meet.. I.S.R.S., Pub!. Servo Smithsonian Contr. Mar. Sci. Geo!. Lux. 29: 161-169. Rützler, K. & 1. Macintyre. 1982. The habitat distribution Antonius, A. 1996. Sinai coral reefhealthsUTvey II: Gulf of and community structure of the Barrier Reef complex Aqaba, Straits ofriran, and Ras Mohamed. Report to at Carrie Bow Cay, Belize. p:9-45. In K. Rutzler & l. RasMohamed Nat. Park Serv., Sinai, Egypt. 29 p. Macintyre (eds.).The Atlantic Barrier Reef Ecosystem Ballesteros, E. 1994. New records of benthic marine algae at Carrie Bow Cay, Belize, 1. Smithsonian Contr. Mar. from Mauritius (IndianOcean). Bo!. Mar. 37: 537-546. Sci. Ballesteros, E. (in press). The degradation of the coral reef Rützler, K. & K. Muzik. 1993. Terpios hoshinota, a new ecosystem in Mauritius (lndian Ocean): the role of cyanobacteriosponge threatening Pacific reefs. a1gae. Facies pp:395-403. In M. J. Uriz & K. Rützler (eds.). Recent Advances in Ecology and Systematics of Sponges. Bryan, P. G. 1973. Growth rate, toxicíty anddistribution of Scientia Marina. Barcelona. the encrusting sponge Terpios sp. (Hadromerida. Suberitidae) in Guam, Mariana Islands. Micronesica 9: Vincente, V. P. 1978. An ecological evaluation of the West 237-242. Indian demosponge Anthosigmella varians (Hadromerida: SpirastreJlidae). Bull. Mar. Sci. 28: Goreau, T.J., J. Cervino, M. Goreau, R. Hayes, M. Hayes, 771-777. L. Richardson, G. Smith, K. DeMeyer, 1. Nagelkerken, J. Garzón-Ferrera, D. Gil, E.e. Peters, G. Garrison, Vincente, V. P. 1990. Overgrowth activity by the encrusting E.H. Williams, L. Bunkley-WilIiams, C. Quirolo, K. sponge Chondrilla nucula on a coral reef inPuerto Rico. Patterson, J.w. Porter & K. Portero 1998. Rapid spread pp:436-442. In K.Rützler (ed.). New Perspectives in of diseases in Caribbean coral reefs. Rev. Bio!. Trop. Sponge Biology. SmithsonianInstitution. 46: 157-172.