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Home , Acanthopleura granulata, Agaricia, Agaricia agaricites, Amphiprioninae, Amplexidiscus, Anthelia (coral)

Antonius 1/70

Lecture (SS 2000)

Threats to and protection of reefs (gefährdung und schutz von korallenriffen) VO 859403

given by dr. Arnfried Antonius University of Vienna (script compiled by P.Madl)

Part I Definition………………………………………….. 2 Part III zonation……………………………………. 23 Reef building organisms.……...…………………... 2 Deep fore reef, ….……………….……… 24 Characteristics of organic reefs……………………. 3 Reef slope, reef front, reef terrace, …….. 25 Structure of coral reefs……..…………...…………. 4 Fore reef, reef crest……………………... 26 Constructive Components of Reef………………… 4 Reef flat, living coral sub-zone...……….. 27 development…..……………………….. 5 Coral sub zone, ; , shore……… 28 of …..……………………….… 5 Reef Communities………………………………. 29 Development of coelenterata..………………. 6 and the food web……………… 30 Acnidaria ().……………………… 6 The flora of reefs………………...…………... 32 Cnidaria……………………………………… 6 Chlorophyta..……………………………. 32 Morphology of cnidaria……………………… 6 Phaeophyta……………………………… 32 Alternation of generation in cnidaria………… 7 Rhodophyta……………………………... 33 class Scyphozoa..……….....…….…………... 7 …………………………… 33 ……………………. 7 Angiospermia…………………………… 33 order Coronatae…………………………. 8 The fauna of reefs………..……….….………. 34 order Semaeostomae………………….… 8 Porifera………………………………….. 34 order Rhizostomae……………………..... 8 ………………………………… 36 Order Cubozoa…………………….……. 8 Annelida………………………………… 38 class Hydrozoa…………..………………...... 8 Arthropoda……………………………… 41 order Trachylina and Siphonophora…….. 9 Echinodermata…………………………... 42 order Hydroida (Athecata and Thecata)… 9 Other reeffauna………………………….. 45 class Hydrocorallina……..……..…………... 9 Chordata……………………..………………. 46 order Milleporina…………………...…… 10 ………………………………... 46 order Stylasterina…………………...…… 10 Chondrichthyes…………………………. 46 class ……………………………… 10 Osteichthyes…………………………….. 48 subclass ………..…………… 10 in the reef ecosystem…..…………... 51 order Telestacea…………………….…… 10 Reptiles………………………………….. 52 order ……………………..…. 10 Mammalia………………………………. 53 order ……………………….... 11 order Gorgonaceae…………………….... 11 Part IV Environmental parameters………………………. 55 order Pennatulacea……………………… 12 Reef degradation…………………………...….… 55 order Helioporaceae……………….……. 12 Destruction of the reef - abiotic factors....….…… 56 subclass ………..………..….. 12 Chemical factors………………………… 56 order Actinaria…………………………... 12 Physical factors…………………………. 57 order Antipatharia.……………………… 12 Destruction of the reef - biotic factors….….…… 58 order Ceriantharia.……………….……… 13 Coral diseases…………………………………… 60 order .…………….…… 13 Disease working without a pathogen………... 60 order Zoanthidae.……………….………. 13 TBL, WBD…………………………..….. 60 order (madreporina).……….. 13 Disease working witht a pathogen…………... 60 BBD; 61 Part II Scleractinian coral and growth……... 14 RBD, BOC, BAB, BI…….……………... 62 Sexual reproduct. (brooders, broadcasters)….. 14 FI, LOD, YBD, DSD…..……………….. 63 ……………………...… 16 SDR, SEB, PEY……………………….... 64 Anthocaulus, anthocyathus in .…… 17 Diseases involving a combination…………… 64 Growth rates…………………………………. 17 WS………………………………………. 64 Morphology of scleractinian .….………...…. 18 Mutations and other tissue abnormalities..….. 65 Corallite structure and their elements.………. 19 Hyperplasia, neoplasia………………….. 65 Colony growth , forms, and shapes………….. 20 Future outlook…………………………………… 65 Physiology of scleractinian corals...………...…...... 21 Part V References on the web.…………………..……… 67

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 2/70

PART I - Definitions:

Riff1: ein riff ist eine massgeblich von lebenden organismen aufgebaute, meist bankförmige struktur, die vom meeresboden bis zur wasser-oberfläche reicht. Es kann die fysikalischen und ökologischen eigenheiten ihrer umgebung beeinflussen. Die konsistenz ist fest, um den kräften im wasser zu widerstehen und bildet somit einen gegliederten raum für angepasste bewohner (Schuhmacher 1976).

riffe

anorganische riffe organische riffe

andere organismen korallenriffe (siehe “Biologie Rezenter Riffe“ - Velimrov2) Riffbildende organismen: Algen, insbesondere kalkproduzierende rotalgen der familie Corallinacea tragen massgeblich zum aufbau von korallenriffen bei. Fädige blaualgen, bilden polster die in weiterer folge durch sedimentation “verkleben“ und letzendlich versteinern; anhäufungen solcher blöcke bilden riffe; seit dem präkambrium sind die cyanobakterien als baumeister der sogenannten Stromatolithen-riffe bekannt, die in heutiger form in der Bay, vor der westaustralischen küste aktiv tätig sind. Seegräser in verbindung mit riffen ist eher als eine missbräuchliche begriffsverwendung für sogenannte “sedimentfallen” zu verstehen (lt. Moliet und Picard); die sedimentverfestigung wird durch das wurzelwerk des seegrases gefördert - sind daher erst durch die einwirkung mehrerer faktoren in der lage riffähnliche gebilde hervorzubringen; bislang wurden derartige verfestigungen mit 10m mächtigkeit vermessen; da algen und seegräser in den tropen immer anzutreffen sind vermutet man daher nicht zu unrecht dass sandstein-bänke aus seegras-beständen hervorgegangen sein müssen. Polychaeten-riffe3), vertreter einiger gattungen (z.b. Sabellaria und Phragmatopoma) bilden mächtige ansammlungen, welche durchaus die bezeichnung "riff" verdienen. So bildet Phragmatopoma lapidosa in der brandungszone der ostküste ’s bis zu 1m hohe riffe, welche sich mit unterbrechungen über eine länge von mehr als 300km erstrecken. Deren wohnröhren sind mit sand ausgekleidet die durch bioaktivitat der würmer verkrusten. Unter den Sabellariidae sind weiters auch jene vertreter der gattung Sabellarida florensis und S.vulgaris als riffbauer bekannt. Serpulliden-riffe4, zu den riffbildenden würmern zählen auch die borstenwürmer der familie Serpulidae; treten sie in massen auf, so können ihre röhren zu einer kompakten kalkstruktur verbacken. Spirobranchus giganteus ist in massen vor Texas und Florida zu finden (siehe auch fig.1). Gastropoden (vermitiden)-riffe4, rezente und fossile riffe dieser art finden sich nicht nur vor Florida’s küste, sondern auch im östlichen Mittelmeer; Vermetus nigricans baut riffe indem die freischwimmenden larven sich am hartsubstrat festsetzen und gewundene kalkröhren anlegen die sie mit benachbarten individuen verzementieren (siehe auch fig.1) . , wie z.b. austern () und miesmuscheln (Mytilus edulis) bilden ebenso grossflächige muschelbänke, sind aber durchwegs auf gemässigte breiten beschränkt. Korallen, zu den wichtigste riffbildnern zählen jene zu den nesseltieren (Cnidaria) gehörenden steinkorallen (Madreporaria), und andere hermatypische (riffbildendene) korallen, wie z.b. feuerkorallen (familie Milleporidae) als auch hornkorallen (familie Gorgoniidae) sowie weitere vertreter anderer familien. Mithilfe der kalksynthese scheidet der korallenpolypen kalk ab. Die zur kalkbildung nötigen kalzium- 2+ ionen (Ca ) und kohlendioxid (CO2) werden im meereswasser oder im korallenpolypen, von den skelett- aufbauenden zellen zur verfügung gestellt. Daraus wird kalziumkarbonat (CaCO3) gebildet. Dies kann jedoch nur in gewissen massen produziert werden, da das produkt durch massenwirkungs-gesetze - teilweise wieder in lösung geht. Wird aus dem reaktionssystem kohlensäure (HCO3 ) entzogen, kann vermehrt kalk synthetisiert werden. Die zooxanthellen übernehmen diese funktion, sie “saugen” CO2 vom stoffwechsel der korallen und verwenden es für ihre fotosynthese. Mit hilfe der zooxanthellen können korallen ihre kalkproduktion um ein vielfaches erhöhen (see p22 figure 41a).

Kurz einige begriffe aus der paläontologie die in der riffbildung eine rolle spielen: BIOHERM = a mound, dome, or reef-like mass of rock that is composed almost exclusively of the remains of sedentary marine organisms and is embedded in rock of different physical character (riffartig die hügelförmig oder linsenförmig ist - streng organisch entstanden; durch einlagerung organischer strukturen ins gestein). BIOSTROM = refers to a flat bed of often in-situ skeletal organisms without significant relief; riffbildung die ausschliesslich durch sedimentäre organismen herrührt; streng genommen handelt es sich dabei um eine geschichtete struktur (z.b. durch muscheln bewerkstelligt) die nicht hügel- oder linsenförmig aufgeschichtet ist. http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 3/70

The map (adapted from Jaap &Hallock, 1990) shows the different kinds of reefs in Florida and their locations. It must be noted that the habitat distribution is very patchy in each area. In southwestern Florida, the Vermetids are mainly located in the Ten Thousand Islands area but also extend intermittently along the western coast of Florida as far as Sarasota. However, they are not found in Florida Bay or the Keys, but a small colony has been reported on the old coaling piers at Fort Jefferson in the Dry Tortugas. Some researchers have reported in the literature that they consider the that is found in the “Ten Thousand Islands” area are extinct, as the reefs were formed during the last interglacial period that drowned the beach ridges that make up the present-day islands.

Foraminiferen-riffe5 sind überwiegend azoo- Fig. 1 Serpulid- and Vermitid-reefs4 xanthellaten und daher auf tiefere gewässer beschränkt; lediglich Marginopora vertebralis ist als eine der wenigen vertreter auch in der eufotischen zone zu finden und wird durch die aktive mitwirkung der zooxanthellaten besonders gross und kann somit regelrechte foraminiferen-bänke aufbauen. Fig. 2 Marginopora vertebralis

Ahermatypische korallen (frei von zooxanthellaten), beispielhaft einige vertreter: Cladocora cespitosa6, eine im mittelmeer ver- tretene art baut monospezifische bänke auf. • Lophelia pertusa7, ist ein biohermer vetreter und bildet bestände die einige 100m lang werden können; ist in allen ozeanen vetreten und geht in tiefen bis zu 100m. • Oculina varicosa8, kann mit oder ohne ihr auslangen finden; unter mitwirkung der zooxanthellen ist sie am riff- Fig.3b Lophelia pertusa aufbau beteiligt, bei abwesenheit ist sie Fig.3a,Cladocora meist in einigen 100m tiefe als buschig- cespitosa verzweigte “dickichte” in atlantischen gewässern vorzufinden. ahermatypische korallen- Alle andere tiefsee-korallen (bis in 1000m tiefe) riff-strukturen: sind ahermatypisch (azooxanthellat). Fig.3c Oculina varicosa Charakteristika von organischen riffen; • gebaut / gebildet von lebenden organismen; • ständige selbsterneuerung (“selbstreparatur” - see also p55, reef degrdation); • errichten vorwiegend bankförmige strukturen; • die vom meeresgrund bis an die wasser-oberfläche reichen können; • und hinreichend fest sind um der wellen/brandungs-aktivität widerstehen zu können. Fig.4 Tridacna gigas Lediglich die korallenriffe sind gross und fest genug um aus ozeanischer sicht den lebensraum zu beeinflussen indem sie durch aminosäure-produktion (biochemisch) und absorption von nitraten, fosfaten (chemisch) die salinität vorort beeinflussen; durch deren enormen ausmasse beinflussen derlei riffstrukturen die lichtverteilung am riffkörper, wogengang, wasserströmungen, wassertemperatur und somit indirekt den pO2-gehalt des wassers, (allesamt fysikalisch); daraus resultiert eine ökologische zonierung die schutz für jungtiere, unterschlupf und nischen für adulttiere bzw. generell neue lebensräume auch für höhlen- und lochbewohner schafft (see also p23, reef zonation). Riffe sind durchwegs auf nährstoff-arme, kristallklare gewässer beschränkt, und produzieren doch soviel an mehrbedarf um auch andere lebewesen mehr oder weniger direkt zu versorgen. http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 4/70

In vielen bereichen der erde kommen den korallenriffen eine weitere funktion zu - durch die zerstörung vieler saum- und konturriffe geht die wellenbrechende funktion eines gesunden riffkörpers verloren; in folge dessen kommt es zu verstärkter küstenerosion. In sofern beeinflusst ein degradiertes riff auch das küstennahe ökosystem an land. Ein mangrovengürtel kann nur in beruhigten küstennahen gewässern spriessen - ein vorgelagertes riff ohne wellenbrechende funktion setzt die küstenvegetation einer vermehrten brandung aus, wodurch es über kurz oder lang zum rückzug des mangrovenbestandes kommt (see p28, reef zonation).

Aufbau von korallenriffen: steinkorallen sind nur ein teil der vorkommenden bausteine; • in den tropen kommt vieler orts auch der Tridacna gigas9 eine tragende rolle zu; • das füllmaterial ist im wesentlichen kalksand (aus erodiertem bzw; abgestorbenem, biogenem ursprung, wie z.b. schwamm-spikel, mollusken, echinodermaten, korallensubstanz, etc.); papageienfische (Sparidae sp.) weiden korallen der zooxanthellen wegen ab; drückerfische ernähren sich von seeigeln, krabben, muscheln und scheiden gleichfalls das zermahlte kalksubstrat wieder aus; bohrschwämme und seeigel tragen wesentlich zum substratabbau am riffkörper bei (see p57, bioerosion); • als bindematerial (kleber) sind inkrustierende corallinacea (kalk-rotalgen, wie Porolithon, Melobesia) tätig; aber auch foraminiferen (Hamotrema rubra) und bryozoen erfüllen diese funktion;

Constructive components of a reef (see also p29 or Velimirov p16 .... /riffe-bv.pdf) 1. Foundation: sedentary organisms (diatomea, ciliates, foraminifers, corallinaceae, , , etc) form the solid and stable foundation on which the reef system can flourish. A principal requirement for a reef is the ability to maintain a strong substrate or base on which subsequent growth can develop. In many cases, after major tropical storm events (cyclones = typhoons = hurricanes), the remainder of the reef may comprise of only this solid foundation. • Growth of rigid, interlocking structure. • Skeletal structures often remain in growth position. • Only a surfacial veneer is alive. 2. Framework Components: much like the steel girder system of a skyscraper, the framework of the reef allows for rapid upward growth of the reef into shallower water. A common example of the type of coral that fills this role is A. palmata (Caribbean ). Note that the shape that this coral develops is in direct response to the nature of the energy across the reef (see p. 26, fore reef). • Cnidaria / class Anthozoa / subclass Zoantharia / order Scleractinia: stony corals; class Hydrozoa / order Milleporina: hydrocorals; • phylum Porifera () / class Sclerosponges or coralline sponges. 3. Encrusting Components: secrete calcareous, encrusting cement to add additional strength to the reef structure. Upon this framework, corals, sponges, hydrozoans and bryozoan coat the surfaces. If one were to peer into the crack and crevices amongst the framework corals, new and diverse worlds of organisms occupy this niche (or space) with the environment. As we move up into the highest energy parts of the reefs we find that this region is dominated by encrusting growth forms. Although technically not encrusting, the hydrozoan Millipora (firecoral) forms complex honeycomb like structures which are capable of withstanding extreme energies associated with the rim or crest of the reef. At this site, breaking waves produce the highest energies associated with the reef system. • phylum Rhodophyta: red or crustose ; • phylum Foraminifera: encrusting foraminifers such as Homotrema; • phylum ; • phylum Annelida: serpulid worms; • phylum Mollusca: vermetid gastropods. Fig. 5a dynamik der faciesbereiche eines karibbischen riffes 4. Bafflers and Binders for soft tissue intergrowth; flexible seafans, grasses, seawhips, and algae locally slow the speed of moving currents above the reef. As these waters slow in speed, material carried in suspension settle out upon the reef surface (sediment trap). This sedimentation leads to the upward accretion or growth of the reef system. • phylum Porifera: encrusting, massive forms • phylum Coelenterata / subphylum Cnidaria / class Anthozoa subclass Alcyonaria: gorgonians, soft corals / subclass Zoantharia: zoanthids, anemones • phylum Urochordata: encrusting, colonial tunicates http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 5/70

Korallenriff-entstehung11 (see also Velimirov script2): Das riff ist ein dynamisches system, welches ständigen veränderungen unterworfen ist (substrat-aufbau muss dem substrat-abbau überlegen sein, sonst kommt es längerfristig zu einem “give-up reef” - ist speziell im zuge der globalen klimaerwärmung relevant wenn “catch-up“ und “keep-up reefs” durch erhöhte bioerodive aktivität und ungünstige abiotische bedingungen zu ersteren verkommen); dazu müssen verschiedene prozesse zusammenspielen, die nachfolgend erläutert werden. Damit sich eine korallenkolonie entwickeln kann, muss zunächst ein primärpolyp gebildet werden. Diese siedeln sich auf festem substrat an oder aber auf abgestorbenen korallenkolonien; nur korallenpolypen, die sich in unzugänglichen ritzen befinden und vor fressfeinden geschützt sind, können sich weiterentwickeln. Durch hoch- und seitwärtswachsen (knospung) und ständige zusiedlung vergrössern sich die einzelnen primärpolypen, bis sie sich vereinigen und emporwachsen können. Freiliegende hohlräume werden rasch zusedimentiert und durch die aktivität von kalkalgen verfestigt, wodurch eine erfrolgreiche neu-besiedelung gewährleistet ist. Voraussetzung für ein weiteres erfolgreiches wachstum ist seichtes, klares wasser und genügend licht. Prinzipiell geht das wachstum jedoch auf die anreicherung von abgeschiedenem kalk zurück; durchschnittliche vertikale wachstumsraten liegen bei 1cm/jahr. Das an der riffkante abgebröckelte kalkmaterial bildet eine schutthalde auf dem sich, wie beschrieben, neue korallenstöcke entwickeln können. Fig.5b riffentstehung

Walker-Alberstadt Model of Reef Succession10) Pioneer Stage sediment accumulates in mounds organisms collect around mounds Colonization Stage substrate is stabilized by cementer organisms crest is built up by framework Climax Stage structure influences wave patterns Lateral Zonation - communities diversify and sediments differentiate

Coral - what is a coral? The phylum Coelenterata (Cnidaria) consists of aquatic, largely marine, solitary and colonial, usually colorful animals ranging in size from a few mm to 2m in length. Included in this phylum are the jelly fish, the sea anemones and the corals. This phylum represents an important step in the evolution of more complex animals. Im umgangsprachlichen gebrauch wird stattdessen gerne der begriff des korallentieres benutzt; unter diesem oberflächlichen allgemein-begriff verbergen sich neben den scleractinidae (welche aragonit-CaCO3 prezipitieren) mehrere verschiedene sedentäre tiergruppen; • falsche korallen sind den steinkorallen äusserlich sehr ähnlich, bilden aber kein CaCO3-skelett aus; • weichkorallen, lederkorallen (Alcyonaria), die blumentiere unter den korallen bilden kein festes skelett, es besteht nur aus einzelnen kalzit- skleriten; • hornkorallen, edelkorallen (Gorgonaria) die tiere besitzen ein festes endoskelett; • dornkorallen, schwarze korallen (Anthipatharia), kleine dornen, die auf dem schwarzen, verhornten (jedoch nicht verkalkten) ectodermalen skelett aufgelagert sind. • Alcyonacea, (rote, blaue korallen) mit namentlich zwei vertretern musica und coerulea; • Milleporina (feuerkorallen) meist koloniebildende polypengeneration im generationswechsel mit der medusengeneration; • koralline Rhodophyta (Corallinaceae, kalk-rotalgen) eine zu den algen gehörende pflanze die in der lage ist loses substrat in folge ihres metbolismus zu verfestigen;

auszug aus der systematik der korallentiere12 Superphylum ------Coelenterata------Phylum ------Cnidaria------Class Hydrozoa Scyphozoa ------Anthozoa------Cubozoa Subclass ↓ ↓ Octocorallia Hexakorallia Legende: ↓ ↓ Coenothecalia 1-fach unterstrichen: gruppe Alcyonaria enthält arten mit Gorgonaria rudimentärem skelett; Pennatularia Order Hyroidea Stauromedusae Coenothecalia Actiniaria 2-fach unterstrichen: gruppe Trachylina Coronatae Telestacea Madreporaria* enthält arten die riffbildend Siphonophora Semaeostomeae Pennatulacea Corallimorpharia tätig sind; Milleporina Rhizostomae Alcyonacea Anthipatharia Stylasterina Gorgonacea Ceriantharia *) ahermatypische Zoantharia Madreporaria sind (extinct) azooxanthellaten, daher nur Familie Hydroidea Rhizostanae Helioporidae Scleractinidae Cubomedusae bedingt riffbildend; Hydnocorallina Semaeostanae Tubiporidae (s. references13) Milleporidae Coronatae http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 6/70

Development of coelenterata31: der bauplan der Coelenterata ist in der regel nur aus zwei schichten zusammengesetzt - das ectodermale und endodermale häutchen; das mesoderm ist nicht entwickelt. Dadurch ergibt sich bei vielen arten ein sehr eigenartiges verhältnis von körper- zu wassermasse, die bei den medusen gar zu 99% wasseranteil aufweisst. Protostomia ("first mouth") are so called because the mouth develops from the first opening into the gut (blastopore). The body cavity or coelom forms from a split in the embryonic middle tissue (mesoderm). Nach der gastrulation (a process by which cells of the blastoderm are translocated to new positions in the embryo, producing the three primary germ layers), setzt sich die gastrula mit dem aboralen pol an das substrat fest.

Fig. 6 Cross-sections of a juvenile (Megalactis sp.) with three cycles of mesenteries: at left a section at the level of the actinopharynx, at right a section nearer the base. (1) Indicates primary mesenteries, of which there are six pairs; (2) indicates secondary mesenteries, of which there are six pairs; and (3) indicates tertiary mesenteries, of which there are 12 pairs. In this example, the primary mesenteries are complete (they connect to the actinopharynx, as in the left-hand image), whereas the secondary and tertiary mesenteries are incomplete (they do not connect to the actinopharynx). Polyps of some species have fewer cycles of mesenteries and some have many more, and the number of cycles of complete mesenteries varies; these are all characters of systematic importance.14

Acnidaria15: die rippenquallen (Ctenophora) tragen keine nesselzellen und wurden daher einem eigenen stamm, den Acnidaria zugeteilt, um sie von den nesseltieren abzusetzen. Ctenophores (Greek for "comb-bearers") have eight "comb rows" of fused cilia arranged along the sides of the , clearly visible along the red lines in these pictures. These cilia beat synchronously and propel ctenophores through the water. Some species move with a flapping motion of their lobes or undulations of the body. Many Fig. 7 Ctenophora ctenophores have two long , but some lack tentacles completely. Ctenophores, variously known as comb jellies, sea gooseberries, sea walnuts, or Venus's girdles, are voracious predators. Unlike cnidarians with which they share several superficial similarities, they lack stinging cells. In order to capture prey, ctenophores possess sticky cells called colloblasts attached to each of their tentacles. In a few species, special cilia in the mouth are used for gelatinous prey.

Cnidaria16: the name Cnidaria comes from the Greek word "cnidos", which means stinging nettle. Casually touching many cnidarians will make it clear how they got their name when their nematocysts eject barbed threads tipped with poison. Many thousands of cnidarian species live in the world's , from the tropics to the poles, from the surface to the bottom. Some even burrow. A smaller number of species are found in rivers and freshwater lakes. There are four major groups of cnidarians: Anthozoa, which includes true corals, anemones, and sea pens; Cubozoa, the amazing box jellies with complex eyes and potent toxins; Hydrozoa, the most diverse group with siphonophores, hydroids, fire corals, and many medusae; and Scyphozoa, the true . Cnidarians are incredibly Fig. 8 Fungiid diverse in form, as evidenced by colonial siphonophores, massive medusae and corals, feathery hydroids, and box jellies with complex eyes.

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 7/70

Nematocyst16: these organelles originating from embryonic cells, contain a coiled thread-like filament that can be rapidly everted like a harpoon when triggered (via a cnidocil) by contact with an object or a chemical stimulus. In many cnidarians, these nematocysts contain powerful venoms (in some species even lethal for humans) that can be used for defense or to capture prey. In order to efficiently capture and paralyze the prey, nematocysts are found in batteries all over the ectoderm. Trichocysts17 are microscopic dart-like structures used for defense Fig. 9 Nematocyst by ciliates and some cnidarians. Spirocyst: ist eine sonderform der trichocyten in der um das steife zentralrohr ein klebriger faden gewunden ist. Fig. 8 Trichocyst

Alternation of generation among cnidarians18: bei der fortpflanzung durchlaufen die nesseltiere einen sogenannten generationswechsel (two-stage lifecycle). Larve, und die glockenartige meduse, die uns als "qualle" geläufig ist. Im unterschied zur metamorfose bei insekten kann sich das individuum jedoch ungeschlechtlich vermehren, noch bevor es das endstadium erreicht: es teilt einfach mini-sprösslinge ab (ephrya), die wie knospen wachsen oder quer abgeschnürt werden (strobilation). Allerdings durchlaufen nicht alle nesseltiere die gleichen stadien, und manche kommen auch ohne generationswechsel aus. Class Scyphozoa32 (Gk. skyphos, cup; zoon, animal) inkludiert die gruppe der echten quallen bzw. scheibenquallen; sie entstehen aus dem polypen durch eine besondere art der knospung, der strobilation, am oberen ende eine reihe junger medusen (dominierende generation), Fig. 10 Lifecycle of Cnidaria die bei ihnen Ephyra-larven genannt werden. Diese entwickeln sich weiter zu geschlechtsreifen quallen; Scypho-medusen besitzen als gravitationsdetektor statocysten und auch rudimentär ausgebildete augen, jedoch kein velum. Vom polypen bleibt ein rest-körper haften, der sich regeneriert und erneut strobilieren kann - er ist potentiell unsterblich. Rund 200 arten sind weltweit bekannt. Zu ihnen gehören die fahnenquallen wie die blaue haarqualle (Cyanea lamarkki) und die gelbe (Cyanea capillata). Die meduse dieses als " feuerqualle" bekannten tieres erreicht in der Arktis einen durch-messer von mehr als 2m. Die ohrenqualle (Aurelia aurita) verträgt sowohl grosse schwankungen der temperatur wie auch des salzgehalts im wasser und ist daher in allen weltmeeren verbreitet. Sie ist leicht kenntlich durch vier violette, ringförmige geschlechts-organe, die "ohren". Die 21 leucht-qualle (Pelagia noctiluca) hat die polypenform als anpassung Fig. 11 luminent Scyphozoa an das hochseeleben völlig unterdrückt. Auffällig sind auch die kompakt gebauten wurzelmund-quallen (Rhizostomea). Deren medusen kommen auf einen durchmesser von bis zu 90cm. • Order Stauromedusae33 (Gk. stauros, stake; medusa, one of the Gorgons of Gk mythology having snakes for hair) include stalked jellies (stiel- oder becherquallen): not all scyphozoa live the mobile free-swimming existence. An attractive group known as stauromedusae have forsaken the medusa stage and live their entire lives associated with the . Their planula larvae are crawlers rather than swimmers. After selecting an appropriate spot, the planula attaches and eventually develops into a polyp- like form. Rather than strobilating like other scyphozoan polyps, it develops directly into the stalked adult, thus retain their sedentary lifestyle. Like coronate medusae, these scyphozoans Fig. 12 quadricornis; retain vertical internal septa as adults. charakteristisch sind die vier Substrates such as seaweed and rock serve as sites for attachment. armpaare. Small are the favoured prey, captured by 8 clusters of knobby tentacles. The wider portion of the body attached to the stem is known as the calyx. Many Stauromedusae have cryptic colors and patterns and are difficult to find in their natural habitats. The photographs show the typical stauromedusan body form.

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• Order Coronatae (L. coronatus, crown) die kronenquallen: the coronate scyphomedusae include some of the most stunning of all the jellies. Within Monterey Bay this group is nearly entirely found only in deep midwater habitats. Among the coronates, Periphylla periphylla is the only species known to be holo- planktonic without any kind of sessile polyp stage. It also lacks the Ephyra stage and does not produce planula larvae like other scyphozoans. Periphylla has a groove in the exumbrella (coronal groove) that probably provides some flexibility to the relatively stiff bell. The bell may reach up to 20cm in height, has 16 lappets Fig. 13 Periphylla periphylla around the margin, and is topped off by a conical apical tip. The tentacles are stiff and 12 in number, and often held In an upward position. They form groups of three that alternate with the 4 rhopalia. Through the transparent bell is seen a strikingly beautiful deep reddish-brown stomach area. Presumably the brilliant pigmentation in this and other deep-water jellies masks the light produced by ingested bioluminescent prey. Periphylla is a vertical migrator, rising to shallower depths at night to feed on and other crustaceans. It is found throughout the worlds oceans, typically below 900 meters in Monterey Bay and as deep as 7000 meters in other areas, but potentially at the surface in higher latitudes. Periphylla may reach much larger sizes in Antarctic waters compared to temperate latitude populations. This species may be the most abundant, widely distributed deep-water scyphozoan, and is commonly collected in midwater trawls by scientists. • Order Semaeostomae34 (Gk. semeia, standard; stoma, mouth) includes moonjelly (ohrenqualle): moon jellies differ from other large scyphomedusae in that they lack the long, potent stinging tentacles that people generally associate with jellyfish. Instead, the moon jelly may capture food on the surface of the bell using mucus to ensnare prey. Cilia transport the food to the bell margin and tentacles, where it is passed to the frilly, conical manubrium. With its high surface area, the manubrium also probably functions directly in the capture of prey. The 4 horseshoe-shaped stomach pouches are readily visible at the top Fig. 14 Aurelia aurata center of the bell, as are the purplish gonads immediately beneath. When a moon jelly has had a hefty meal, it's easy to see food packed in the stomach pouches.Hundreds of fine, relatively short tentacles line the bell margin. The sting of this jelly is mild and most people have only a minimal reaction to it, if at all. The bell is a striking translucent white, diameter up to 40 cm, and may be tinged with pink or lavender. It is marked by 8 lobes, each with a notch so that there appears to be 16 lobes, and 8 rhopalia. are readily distinguished since females hold the fertilized , which appear as whitish-gray clumps on the manubrium. Males may sometimes be seen with long filaments trailing from the oral arms. • Order Rhizostomae35 (Gk. rhiza, cube; zoon, animal) the “up- side-down” jelly (wurzelmund-quallen): a yellow brown jellyfish with a circular body. Oral arms are a dark brown color. Cassiopeia sp. live in warm, shallow waters. Many are found in mangrove bays. Cassiopeia sp. lays upside down in order to expose its symbiotic algae to the sun (make their own food from light energy via ). They shoot out nematocysts and mucous (stinging stuff) to catch its prey; thus are mildly toxic and Fig. 15 Cassiopeia sp. contact with them causes a rash. Class Cubozoa36 (Gk. kybos, cube; zoon, animal) the distinct box jellies (würfel- oder feuerquallen): bei den würfelquallen (cubomeduse) reift die planula zu einem winzigen cubopolypen heran. The bell of these primarily tropical jellies is indeed somewhat cuboidal with 4 flattened sides. Box jellies tend to be transparent and can be quite difficult to see in the water, even with large individuals. The bell margin lacks any and has a velum-like rim similar to that in hydromedusae. Another characteristic, the possession of gastric filaments, (similar to scyphozoans). A , or group of tentacles Fig. 16 Carybdea marsupialis originate from each of the 4 corners. One of the more remarkable

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aspects of box jellies is their possession of a complex eye within each of the 4 rhopalia that enables them to track moving objects and quickly respond to changes in light intensity. Cubozoa are elaborate swimmers. Although the polyp stage is subordinate, they can reproduce asexually by budding to form new polyps. They do not strobilate, however, and instead each develops directly into a small medusa (polyp metamorphoses completely to axial-symmetry). Among the box jellies is the notorious sea wasp of Australia (Chironex fleckeri37 and Chiropsaimus quadrigatus), which can have a fatal sting. Class Hydroza (Gk. hydra, water serpent; zoon, animal): sie gelten als die am höchsten entwickelte form unter den nesseltieren; rund 3000 bekannten arten gehören dieser klasse an, von denen 700 medusen bilden. Aus den polypen (dominierende generation) wachsen durch knospung ganze kolonien oder "stöcke". Die freischwimmenden werden meist nur wenige zentimeter gross. Im gegensatz zu den Scyphozoa besitzen Hydrozoa ein velum. Zu ihnen zählt der süsswasser-polyp Hydra. In die klasse der hydrozoen werden auch die staatsquallen (siphonophora) eingeordnet, die aus vielen einzelpolypen oder -medusen bestehen. Die etwa 150 arten können von wenigen mm bis zu mehreren metern lang sein. Fig. 17 Hydrozoan body plan • Order Trachylina19 (Gk. trachys, mrough; L. linum, flax); planktonic hydreomedusae with no polypoid stage; this order contains perhaps the most primitive members of the

class, Aglaura. These animals Fig. 18a Voragonema usually swim with their buccal pedunculata (nat. size cavity showing upwards. approx. 2cm in diameter) • Order Siphonophora20 (Gk. siphon, tube; pherein, to bear); includes the Portugese Man of War Jellyfish (Physalia physalis30); its tentacles can exceed 16m in length, but do not pose a lethal threat to humans. The “Portuguese Man of War” is a floating hydrozoan colony. Locomotion is generally passive, driven by wind and current. It is actually a colony consisting of four polyps: a pneumatophore, or float; dactylozooids, or tentacles; gasterozooids, or siphons; and, gonozooids. Nematocysts Fig. 18b Physalia physalis (stinging cells) are located in the tentacles. An important aspect of the Man of War's behaviour is the symbiotic relationship between the Man of War and the Nomeus (a minnowlike fish), a clownfish (commonly called the Man of War fish), and the yellow-jack. These live within the tentacles of a Physalia and are rarely seen elsewhere. The fish, particularly the clownfish, produce slimy mucus that causes the Man of War not to fire its nematocysts. • order Hydroida24,29 (Gk. hydra, water serpent; eidos, form); kommen in 2 unterordnungen vor: i) ANTHOMEDUSAE (Athecata) i) LEPTOMEDUSAE (Thecata) Dominierend ist das polypenstadium ?; bildet Fig. 19a Regeneration of hydroids Fig. 19b Body plan of hydroids sehr kleine weissliche polypen aus die einer feder sehr ähnlich sind, jedoch stark nesselnd wirken25. Im medusenstadium sind sie als kaum sichtbar nur im mikroskop zu erkennen und führt so zum begriff des “nesselnden wassers“.

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Class Hydrocorallina (Gk. hydra, water serpent; korallion, coral); it includes Milleporina, Stylasterina, Trachylina; the members of this class, which form colonies with massive skeletons of aragonite (calcium carbonate). These two orders differ in details of skeletal construction and dactylozooid (prey-gathering polyp) morphology. Sometimes grouped together in the family Hydrocorallidae26; both kind display a reduced meduse stage with the dominant polyp stage: • Order Milleporina27 (L. mille, thousand; poroa, pore) are known as "fire corals" for their coral-like growth and their painful sting; They are easily mistaken for true corals, whereas hydrocorallina are colonial hydrozoans and secrete a massive calcareous skeleton with a smooth surface; the polyps are connected by gastrovascular canals. Hydrocorallina posses sensing dactylozooids that bear clusters of nematocysts able to deliver a powerful sting and feeding gastrozooids with tentacles. Hydrocorallina are common components of coral reefs and even house zooxanthellae (symbiotic algae residing in their tissue that photosynthesizes). During their reproductive stage, they develop minute free- Fig. 20 Milleporidae swimming medusae which are produced in sexual generations; asexual "breaking" and splitting also generate "new" individuals. Hierbei dominiert die polypengenration wohingegen die medusen-generation wie bei den hydroida nesselndes wasser generiert. • order Stylasterina (lace or rose corals)28: ist eine kleine hydno- koralle die meist im schattigen bereichen des riffes anzutreffen ist; sie ist besonders auffällig durch ihr stark intensiv violett gefärbtes äusseres erscheinungsbild.

Class Anthozoa (Gk, anthos, flower; zoon, animal) are solitary polypoid Fig. 21 Stylasteridae cnidarians which lack a medusoid stage. The mouth opens into a pharynx and gastrovascular cavity partitioned by mesenteries. Subclass Octocorallia38 (Gk. okto, eight; korallion, coral) Although commonly called "soft corals," the Octocorallia are not close relatives of the scleractinians, or "true corals“ living today. Unlike true corals, which have hexaradial symmetry (multiple cycles of six), octocorals have 8-fold radial symmetry. In addition; the small branches off of the main tentacle to give octocorallia a more or less feather-like appearance. All octocorals are colonial polyps, and in some, such as the Pennatulacea, the polyps are specialized for various functions. Except for the "" and "organ-pipe corals," few octocorals produce substantial calcite carbonate skeletons; hence, the name "soft coral" for many of them. However, most octocorals form spicules within their tissues, and some produce calcified holdfast structures or long, rodlike internal supports; these parts can be preserved as . Octocorals are traditionally divided into six orders: • order Telestacea39 (after the Telestos) include the branched pipe corals and is a small group; colonies occur as simple or branched stems arising from a creeping giving rise to large upright polyps from which smaller, lateral polyps can arise, giving the whole colony a tree-like appearance. The spicules are united through calcareous secretions forming a skeleton (Hyman 1940). Although rarely imported due to their fragility, according to Wilkens and Birkholz (1986) these corals do well under the proper conditions and some species may be photosynthetic, while others need to be fed planktonic foods. • order Alcyonacea40 (after the genus Alcyonium) inkludiert die lederkorallen und andere weichkorallen; hierbei sind die polypen in die elastische mesogloea des zentralkörpers eingelagert, wobei Fig. 22 Stylatula sp. with a sand letzterer durch spikel verfestigt ist. It contains all the most dweller (slug) Armina sp. on top familiar genera of soft corals, such as Cladiella, Lobophytum, Sarcophyton, Sinularia, Anthelia, Xenia, Capnella, , Lemnalia, Litophyton and Nephthea. All of these genera, with the exception of Dendronephthya, have zooxanthellae. Alcyonacea have fleshy or leathery colonies that tend to be irregular in shape, with various lobes or finger-like projections. Some resemble large toadstools (e.g., Sarcophyton and Lobophytum), while others are more tree-like in shape (e.g. Dendronephthya and Litophyton). Dendronephthya is especially Fig. 23 Muricea sp. http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 11/70

conspicous as it is almost transparent with soft hues while its spicules are vividly colored. Members of these genera are limited to the Indo-Pacific region. Anthelia and Xenia are two genera that are often confused with each other, both genera rythmically open and close their polyps with featherlike tentacles (not to catch planktonic organisms but rather to improve ventilation). Anthelia tend to have longer, more slender polyp stalks than Xenia, and they grow from an encrusting, fleshy mat, whereas Xenia usually have a stalk with polyps arising from the top of the stalk. Xenidae (weichkorallen) bilden zuweilen regelrechte rasen- bestände und wirken durch ihre rhythmischen bewegungen fälschlicherweise als strömungsindikator (vielmehr wird die ventilation gefördert). In diesen tiefen verschiebt sich dass verhältnis zunehmends zugunsten der Alcynacea (weich- und lederkorallen) - ist dieser trend bereits in den lichtdurch- fluteten oberen wasser- schichten zu beobachten, so ist das generell ein zeichen dass es dem riff nicht gut geht! Fig. 23b Dendronephthya sp.41 41 Fig. 23a Sarcophyton sp. with a feeding • Order Stolonifera41 (L. stolon, stalk, fer, to form); the polyps arise singly from a creeping base. Calcareous spicules secreted in mesenchyme; includes the so-called "organ-pipe corals" and tree fern corals. Stolonifera are octocorals whose polyps arise from a creeping base that may consist of separate, flat, root-like structures called stolons, or an encrusting mat. The polyps in most forms consist of two sections. The softer, thinner portion that possesses the tentacles and mouth is called the anthocodia, and this portion can retract into the lower, stiffer non-retractile portion called the anthostele. When retracted, star polyps ( Fig. 24 Tubipora musica spp. and Clavularia spp.) will display this structure nicely. In the Tubipora (red pipe organ coral), the spicules are so dense they fuse together to form a calcareous skeleton; new polyps arise from stolons or from the transverse platforms. • Order Gorgonacea39 (Gk. mythology, the Gorgons who had snakes for hair): horny corals with calcareous spicules and small or minute polyps; it includes sea fans, red coral, sea whips, and sea feathers. Gorgonians have a strong, flexible interior axial skeleton made of a horny material called gorgonin. This skeleton, in the form of rods, provides for greater flexibility and support. The skeleton is surrounded by a layer of tissue in which the polyps are embedded. This tissue also contains numerous conducting tubules and calcareous spicules. Although there are some encrusting and single-stemmed species, the majority resemble trees in their branched appearance. The precious deep- water red and pink corals of the Mediterranean, Japan and Fig. 25a Gorgonaceae40 are gorgonians too but they lack gorgonin, having instead fused calcareous spicules that form the highly prized material from which is made. Photosynthetic Caribbean gorgonians have also gained a great deal of attention from the medical community because they are natural sources of some very interesting anti-inflammatory chemical compounds, such as the prostaglandins (see Faulkner 1992). Entlang des überganges vom weichboden zum riffhang findet man vielerorts peitschenkorallen (Elisella sp.) bzw. Antipatharia (schwarze korallen). Die in diesen tiefen vorherrschende schwache licht-einstrahlung und wasserbewegung Fig. 25b Elisella bedingt eine ausrichtung der sessilen fauna in längsrichtung (quer paraplexauroides zur strömung) um aus dem wasser filtrieren zu können.

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• Order Pennatulacea42 (L. pennatulus, winged); the sea pens have fleshy colonies with primary and secondary polyps; it includes sea pens and sea pansies. As is the case for all octocorals, sea pens are actually colonies of polyps. What distinguishes sea pens is polyp dimorphism (entire organism is laterally symmetric). An apical polyp grows very large and loses its tentacles, forming the central axis. The base of this primary polyp forms a bulb which may be expanded or contracted; the uses this bulb (not visible in the picture to the right) to anchor itself in sandy substrates. Branching off this primary polyp are various secondary polyps. Fig. 26 Sarcoptilon sp. Some, called autozooids, are typical feeding polyps. Others, the larger and fewer siphonozooids, serve as intakes for water, which circulates within the colony and helps keep it upright. Also supporting the colony arecalcareous spicules and frequently a central axial rod of calcium carbonate. In one group of sea pens, called the Subselliflorae, the secondary polyps are grouped into “polyp leaves,” as in the Pacific species of Sarcoptilon shown here. The feather-like appearance of these species gives the sea pens their common name; they look something like old-fashioned quill pens. Most species, however, do not have polyp leaves, and look more like clubs, umbrellas, or pinwheels. • Order Helioporacea39 (Gk. helios, sun; poroa, pore) includes only one genus, Heliopora, the so-called “blue coral” and is limited to the central Indo-Pacific only. This species grows in large brownish or greenish-gray mounds and has numerous delicate white polyps over its surface. The colonies are heavily calcified (aragonitic fibers fused into laminae) and thus appear similar to Millepora. When dead or broken, one can see the blue color of the skeleton caused by the infiltration of iron salts (Hyman 1940). These photosynthetic corals are rarely available, Fig. 27 Heliopora coerulea but they do very well in .

Subclass Zooantharia39 (Gk. zoon, animal; anthos, flower); often termed Hexacorallia (belong to the class Anthozoa); in contrast to Octocorallia exhibit a great deal of anatomical variation, which makes them difficult to describe in general terms. Unlike the octocorals, hexacorals usually have tentacles and internal polyp septa in multiples of six – although exceptions do occur – but never eight. The oral disc has a prominent mouth that may be situated on a protuberance or have a protruding margin (Hyman 1940). The tentacles of the polyps do not have pinnules as in the octocorals. There are at present 6 recognized orders: Actiniaria, Antipatharia, Ceriantharia, Corallimorpharia, Scleractinia and Zoanthidae. • Order Actiniaria42 (Gk. aktinos, ray) it contains all the organisms we call sea anemones. They are quite diverse in their appearance, ranging in size from a few cm to more than 40cm in diameter (in the case of ). The bottom of the anemone is formed into a disc (pedal disc = fuss-scheibe) with which it attaches itself to the substrate or even enables it to crawl along the surface. The other end contains the mouth (oral disc) and is situated in the middle of a broad oral disc surrounded by stinging tentacles of varying length and shape, depending on the species. Many species of tropical anemone contain zooxanthellae, but most temperate species do not. Actinarian anemones can reproduce either sexually or asexually, but they do not form true colonies with permanent tissue Fig. 28 Sea anemone connections between members, unlike the superficially similar zoantharians. • Order Antipatharia (Gk. antipathies, ) contain the well-known precious black or thorny corals (dornkorallen, schwarze korallen) out of which jewellery is made; usually found at depths greater than 20m to depths of even 100m. These tree- like corals, that may well become 1-3m tall, have a thin chitinous Fig. 29 sp. and black axial skeleton with small thorns made of a material – similar to gorgonin. There is a thin veneer of living tissue from which the simple “nakes” polyps arise. A.subpinnata is the medirerranean representative, while A.dichotoma is found in the Indo-Pacific.

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• Order Ceriantharia46 (Gk. kerion, honey comb; anthos, flower; zylinderrosen): are non-photosynthetic, anemone-like anthozoans that have a muscular, elongated, cylindrical body with a fleshy foot that extends deep into the sand so that the oral end bearing the tentacles extends outward. The tentacles tend to be extremely fine and long, and some specimens of Cerianthus can sting quite powerfully. These anemones are not photosynthetic, and as being carnivors rely on passing prey. There are severel genera, Cerianthus being mediterranean, while Pachycerianthus and Fig. 30 Cerianthus lloydii Arachnantus are found in the Indo-Pacific and the Caribbean respectively. • Order Corallimorpharia45 (Gk. korallion, coral; morph, form): contain the popular mushroom anemones, which are not really anemones – they are also known as “false corals” (falsche korallen) and resemble stony corals, but lack skeletons. Polyps can occur as solitary individuals, or in colonies. The tentacles are usually reduced to knobs or small branched protuberances, arranged around one or more mouths. These anthozoans do contain zooxanthellae. Fig. 31 Corynactis sp. Various genera, such as Actinodiscus, Amplexidiscus, Discosoma, Rhodactis and Ricordea, are included in this order. • order Zoanthidae44 (Gk. zoon, animal; anthos, flower; krustenanemonen): are a small group of solitary, but usually colonial, anemone-like anthozoans in which all members are connected by common tissue; zoanthids lack a skeleton and unlike any other anthozoan internally, have a large number of paired and unpaired septa (Hyman 1940). Zoanthid polyps can occur as single individuals in large groups or they can be joined together by a thin stolon, i.e. a thin or a very thick coenenchyme, from which only the mouths and tentacles are visible (e.g. Palythoa caribaeorum). Fig. 33 Palythoa sp. • Order Scleractinia47 (Gk. skleros, hard) are often termed Madreporinaria (steinkorallen): represent the stony or hard corals. Stony corals are basically anemones that are surrounded by a calcareous skeleton. The polyps can be solitary or they can exist in large colonies joined by a common tissue called coenenchyme. Due to the colonial nature of many stony corals, they can build massive structures that result in the development of entire coral reefs. The majority of stony corals harbor zooxanthellae (thus often termed zooxanthellates) and derive much of their nutritional Fig. 32 Scleractinia requirements from the metabolic products produced by the zooxanthellae, while azooxanthellates do not house these symbiotic .

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PART II - Scleractinian coral reproduction and growth47:

Knowledge of coral reproduction has expanded greatly over the past 10 years into one of most intensely studied aspects of coral biology. Review by Richmond and Hunter 1990 provides overview of status of knowledge. Reproductive data are now available for about 210 of approx. 600 spp. of reef corals. What is most impressive is the variety and versatility of coral reproduction both sexual and asexual.

Sexual reproduction: corals exhibit sexual and asexual reproduction. Unlike asexual reproduction, which produces exact copies of the parent (clones), offers two opportunities for new genetic combinations to occur, a) crossing over during meiosis, and b) b) the genetic contribution of two different parents when an is fertilized by a sperm. The individual coral polyp can be male, female, both or may not be reproductively active at all. If a polyp is just of one then it is termed gonochoric. A polyp that is both male and female is known as a . In hermaphroditic corals; in order to prevent self-fertilization, male and female gametes never mature at the same time. Die sexuelle vermehrung bei den korallen ist eine komplizierte angelegenheit; bis dato wurden keine getrennt-geschlechtlichen polypen in einem korallenstock gefunden ?; die sexuelle vermehrung kann auf zwei unterschiedliche vorgänge erfolgen: Broadcasters: sexual fertilization of released positively buoyant gametes at very specific times so as to ensure fertilization; fertilization is external at the water surface; Many coral species mass . Within a 24 hour period, all the corals from one species and often within a genus release their eggs and sperm at the same time. This occurs in related species of Montastraea, and in other genera such as Montipora, Platygra, Favia, and (Wallace, 1994). In some Montastraea and species, the eggs and sperm are released in a sack. They float to the surface where they separate and fertilization takes place. Intraspecies fertilization is common but mass spawning raises the possibility of hybridization by congeneric species (Wallace, 1994). The zygote develops into larvae called planula which attaches itself to a suitable substrate and grows into a new colony. Brooders: asexually brooded planula larvae may be developed by a kind of budding (internal fertilization, brooding of zygote, and release of planula, vivipary); some species of coral even brood their larvae. The sperm fertilizes the egg before both are released from the coral. The larvae float to the top, settle, and become another colony. Species of Acropora release brooded larvae. Corals start their life as a free-swimming young (after spawning, the planula larvae is only the size of the head of a pin) that are carried by ocean currents. The larvae will drift with the current until it finds a hard bottom to attach itself. Once the larvae attaches to the bottom it quickly changes into a polyp (will never move again). It reproduces by budding (in which an identical polyp sprouts out of the polyp’s side) and by sexual reproduction (in which polyps release eggs and sperm, which mix in the water).

Fig. 34 Life cycle of corals58

Fig. 33 The generalised life cycle of a broadcast hard coral59

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Reproductive variations among scleractinian corals: A. Involves spawning fertilization and production of planula larvae. B. Spawning: seasonal, monthly or annual. C. Annual multi-species spawning occurs synchronously in >140 spp in GBR. • Occurs 5 days after full moon in late spring (neap tides warm waters). • Degree of synchronized spawning may be related to annual temperature range which is greater in GBR than other reef regions; temperature change may provide seasonal cue. • Lunar phase may fine tune the particular night for mass spawning. D. Fertilization can occur externally through free release of gametes (broadcast spawning) or within maternal polyp followed by brooding of larvae. E. In hermatypic corals, spawners outnumber brooders. • typical of corals in buttress and fore reef zones massive colonial forms with indeterminate growth (e.g. Acropora, Montastrea spp. in Caribbean); • broadcasters have high larval mortality but successful recruits can invade new environments with lower competition; • surviving colonies can live 100s of years; • low recruitment rates are acceptable. F. Most ahermatypes are brooders as are hermatypes living in disturbed, nearshore reef zones (e.g. Favia fragum broods embryos for 3 weeks); • zones with high adult mortality require high rates of recruitment; brooding produces mature planulae ready to settle; • brooding also found in spp. A.humilis in shallow reefs and A.agaricites in deeper zones which have high competition for spaces, as well as high rates of bioerosion. G. Hermaphroditism is common in 68% of studied spp. • egg and sperm production can occur on same mesentery or on differentiated mesenteries in same polyp, in different polyps of same colony, or at different times in same colony (i.e. sequential as well as simultaneous hermaphroditism). H. Planula larvae are produced by both sexual and asexual modes of reproduction. • Planula larve are cilliated and up to 1.6mm long. • Some contain zooxanthellae when released from parental polyp. • Some can live in plankton for up to 100 days. • Helix experiment (Sammarco & Andrews) showed limited degree of dispersal from an isolated reef in GBR and control by regional circulation patterns.

Coral spawning56: rhythmicity in moon phase luminance (29.5 day periodicity) appears to be the most important environmental monthly spawning synchronizer. The main annual spawning season inducer appears to be temperature variances. As the annual variation increases, the spawning season will shorten for monthly brooding species whose minimum gonad development temperatures are not attained. Monthly brooders will start to release planula based on the lunar periodicity of the ecosystem. The photoperiod of periodicity combined with annual temperature variances are thus the key elements for the development of mass spawning event. Triggers in coral spawning57: • water temperature • lunar cycle • hours after dawn Steps in sexual reproduction:

Fig. 35c early (top) and later (bottom) Fig. 35a Coral releasing development of planula eggs (top) and sperm Fig. 35b Fertilization at the 52 larvae belonging to Fig. 35d a week old (below) surface (top); eggs and zygotes 52 of Acropora palmata (below)52 Acropora sp. Montastraea faveolata (top, ca. 0.5mm); young polyp settled on a suitable substrate (below)52

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Corals can reproduce also vegetatively. The term asexually can be referred to as vegetative and the term sexually as generative. Through asexual reproduction, a coral can make a clone of itself. The two methods of asexual reproduction are able to eventually give rise to an entire colony. Individual corals can reproduce through by transversal division. In this way, coral colonies are able to live for a few hundred years. Asexual reproduction is thus the main cause of coral growth.

Asexual modes of reproduction to ensure colony growth - budding of polyps from a parent colony. A. “Polyp bailout”: polyp abandons corallite, and re-establishes on a new substratum. B. Fragmentation: colonies broken up during storms can initiate many new colonies. • Common in branching forms. • Important for spp. at limits of distribution where conditions might not favor sexual reproduction or in stressful habitats without optimal regions. C. Colony growth is by asexual multiplication. • Budding of polyps from a parent colony. • Peripheral increase by fission.

Colonies can grow in the following manner: 1) by producing stolons: stolons horizontally grow cell layers. They look like a system of roots that fix the whole colony to substrate. New polyps grow on stolons; 2) by monopodial growth: this term means that the trunk of the colony is made by the oldest polyp. The trunk grows during growth of new polyps. The oldest polyp is always on top of the colony; 3) by sympodial growth: this colony does not produce a trunk. New polyps offshoot along the edges of adult polyps. The youngest polyps are always on top of colony; 4) by dychotomic growth: dychotomic growth means that the corals divide symmetrically. Since all polyps grow simultaneously, neighbor polyps are the same age.

Budding (knospung) 50: the coral colony expands in size by budding. In the process of budding, a young coral individual grows out from the adult (parent) polyp. This is the way a colony grows. Within the reach of the oral disc or beyond the wreath of tentacles on an adult polyp, a daughter polyp forms. The progeny polyp has two cell layers: ectodermis and gastrodermis. As the progeny polyp grows, it produces a coelenteron, tentacles and a mouth. Sometimes, the young Fig. 36 intra- (left) vs. extra- polyp can originate beyond the wreath of tentacles. (right) tentacular budding The distance between the polyps increases which causes development of coenosarc (the common body of the colony). New polyps grow on the coenosarc by producing new coenosteum, the colony’s exoskeleton. Budding may be intra-tentacular, in which the new bud forms from the oral discs of the old polyp, as in sp., or extra-tentacular in which the new polyp forms from the base of the old polyp, as in Montastraea cavernosa. • intra-tentakuläre knospung: zwei gleich grosse tochterpolypen gehen aus einem elterlichen polyp hervor, verbleibt aber noch während der teilung innerhalb des elterlichen tentakelkranzes; bildet in meandrierenden formen ganze polypenreihen; • extra-tentakuläre knospung: die folge-generation geht aus dem elterlichen polypen hervor wobei sich zwei gleichgrosse, neue einzelpolypen entstehen (niemals reihen). • longitudinal division: in longitudinal division, the coral polyp begins to broaden; it then divides into a coelenteron and mesenteries; next, the mouth divides and tentacles encircle the new mouth. The difference from the above is that during budding, the parent polyp produces a smaller polyp, whereas after division, the two polyps are identical. There is no distinction of parent and daughter polyps in a division. Individual polyps divide according to the radial arrangement of septa. Every new part has to complete its missing parts of the body and exoskeleton. • transversal division: individual corals are able to reproduce by transversal division. Polyps and the exoskeleton divides transversally into two parts. One of them has the basal disc. The second has the oral disc. The two new polyps must complete missing parts of the body and exoskeleton in order to function. Fission: some corals (esp. mushroom corals among the family Fungiidae) are able to split into two or more colonies during the early stages of their development (also called strobilization); Fragmentation: last method for coral colonies to propagate is through a process of fragmentation. A piece of colony can actually be broken off to grow a clone.

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 17/70

Reproduction in Fungiidae60: laut Veron (1986) sind wahrscheinlich alle Fungiidae getrennt geschlechtlich, wobei die weiblichen korallen entweder eizellen oder sexuell erbrütete planulae ins wasser entlassen. Viele pilzkorallen (Wood 1983 Heliofungia, alle -, Cycloseris- und Diaseris-arten) besitzen eine eigenartige geschlechtliche fortpflanzung, aus der sogenannte anthocauli hervorgehen. Als anthocaulus wird der sessile, gestielte jungpolyp bezeichnet, der sich aus der festgesetzten planula-larve entwickelt. Anthocauli führen meist ein ziemlich verborgenes leben in strömungsgeschützten, schwach beleuchteten nischen von hardsubstraten. Während des wachstums verlängert sich der basale stiel und verbreitert sich die mundscheibe (= anthocyathus) hutartig - daher auch der name “pilzkorallen”. Mit erreichen eines mundscheiben-durchmessers von maximal etwa 4cm bricht der anthocyathus vom stiel ab und wächst als frei auf dem boden lebende koralle weiter. Der biologische vorteil dieser zunächst sessilen lebensweise dürfte mit dem veränderlichen, sedimentations- und zeitweilig sehr strömungsreichen lebensraum der pilzkorallen zusammenhängen, in dem aus planula-larven entstehende jungpolypen vermutlich geringere überlebens-chancen hätten. Anthocauli können aber auch (bei vermutlich allen Fungiidae) ungeschlechtlich entstehen, in form von kleinen tochterpolypen an der ober- oder unterseite der frei lebenden pilzkorallen. Werden pilzkorallen von grobsedimenten so sehr zugeschüttet, dass sie sich davon nicht mehr befreien können, oder werden geschwächte exemplare von kalk-rotalgen oder anderen sessilen organismen überwachsen, wird dadurch noch lebendes polypengewebe zur bildung von anthocauli angeregt. Doch nicht nur als quasi letzte überlebens-strategie, sondern auch von gering beschädigten oder gesunden pilzkorallen werden hin und wieder solche anthocauli gebildet. Laut Veron soll der anthocaulus-stiel nach ablösung der mundscheibe absterben, doch haben aquarien-beobachtungen gezeigt, dass zumindest bei Fungia spp. sowohl ungeschlechtlich als auch geschlechtlich entstandene anthocauli zu einer mehrfachen mundscheiben- bildung in folge befähigt sind (Stüber 1994; Fossa & Nilsen 1995).

Coral growth rates: Most corals are a colony of many individual polyps, in which each polyp contains dinoflagellates (zooxanthellae) capable of photosynthesis. Without zooxanthellae, the polyps cannot grow fast 2 enough to build reefs (see pages 21, 22). Reef-building corals precipit up to 6 tons CaCO3/(km ⋅day). By night, a polyp captures plankton with its tentacles. By day, the zooxanthellae photosynthesize. The polyp benefits from the photosynthate (product of photosynthesis), and the alga benefits from the nitrogenous wastes of the polyp. There is an intense competition for space. Corals have a rigid pecking order. When more aggressive species recognize less aggressive forms, they send out nasty mesentary filaments as well as sweeper tentacles that wound living coral encroaching on their space. More than 65 species have been found in Caribbean reefs: there are both shallow, fast-growing forms and deep, massive, slow-growing forms (living at a maximum depth of about 30m). The (GBR) of the Indo-Pacific has 350 named coral species.

A. Methods of study 1. Linear or radial growth using stain markers (alizarin), dense banding, etc. ; 2. Colony weight; 3. Radioisotopes; B. Variations of growth form: highly variable but open, branching colonies grow faster in linear dimension than massive colonies with dense skeletons. Branching forms have greater S/V ratio. 1. Branching forms: 100-200mm/yr (staghorn Acropora) 2. Massive colonies: 6-12mm/yr, but colonies (clones) can live for centuries. 3. Using colony weight: branching forms grow faster in proportion to surface area. However, there is no evidence of senility; calcification rate/cm2 is similar for small and large colonies. C. Diurnal, seasonal and long term variations (see Velimirov script2). 1. Diurnal: growth is 14x faster by day in zooxanthellate corals, as determined by Goreau’s 45Ca tracers. 2. Seasonal: grow rates vary reflecting seasonal changes; e.g. in Caribbean Panama. a) Colonies stained using alizarin red to mark wet and dry seasons. b) Over 2 successive years. Wet season rates exceeds dry season rates. About 3 mm/month in wet, versus <2mm/month in dry. Why the difference? c) Wet season May to December; • heavy rainfall, cloud cover; • calmer seas . esp. when ITCZ is south of Isthmus; d) Dry season December to May; • more sunshine, less rainfall; • strong onshore traces from E-NE; • seas are rough, waters turbid; e) During dry season, Porites polyps are retracted more of the time to protect from abrasion. Thus less exposure to light; growth is reduced. During wet, polyps open more of time in calmer seas. f) Other studies have found faster growth correlates with times of greater sunshine, but here other physical factors override effect of solar radiation. 3. Long term: using density bands, long records of growth can be obtained (see Shinn paper). Also recent study of Porites, dating back to as far as 1880. http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 18/70

Morphology of scleractinian corals: Nach erfolgreicher ansiedlung der planula larve auf passendem hardsubstrat, erfolgt die ausbildung einer basalplatte aus 48 aragonit (CaCO3); aufgrund der septenstruktur wird der hohlraum (disseptimente und theca) aufgebaut. Zur erinnerung, die septen sind bestandteile des ektoderms; sie liegen zwischen zwei häutchen (= innenhaut der mesenterien) und sind die Ca-abscheidenden organe des korallengewebes. Sobald die basalplatte angelegt ist, beginnt die jungkoralle mit dem aufbau der seitenwände wodurch der kelch (calix, calice) getrennt wird. Durch einziehen von zwischenwänden (disseptiments) in regelmässigen abständen wird die abgeschiedene struktur zusätzlich stabilisiert; erst jetzt ist die aufbaufase abgeschlossen und die koralle kann mit dem nächsten wachstumszyklus (abscheidung der seiten- und zwischenwand) fortfahren, wodurch die koralle an höhe zulegt. Das organische material unterhalb der aufgebauten disseptimente stirbt dabei ab; folglich ist nur das hauchdünne gewebe (coenosarc) als das biologisch aktive gewebe für den aufbau der skelettstruktur verantwortlich. Koloniebildende arten sind so aufgebaut dass benachbarte polypen durch ein locker strukturierte fülmasse (coenosteum = exothecale disseptimente) getrennt Fig. 37 struktur der korallen sind; je nach art kann es mehr oder weniger mächtig (dünnwandig sein). Das gesamte erscheinungsbild des abgeschiedenen skelettes ist letztendlich artbestimmend, wodurch sich die arten relativ gut (in manchen fällen nicht so leicht) unterscheiden lassen.

Some structural elements of such corals49: • corallite: skeleton of a solitary individual or an individual within a colony; • calice: a cup-shaped depression on the corallite surface; • coenosteum (-a) [or peritheca (-ae)]: skeleton between corallites within a colony; • septum (-a): radially-arranged vertical partition(s) within a corallite; they can be either exsert, insert of even in regard to the corallite wall; • paliform lobe: an exsert protuberance of a septum at the center of the corallite; • wall [or theca (-ae)]: vertical structure enclosing a corallite; • theca: the sheath of “dura mater” which encloses a corallite; • costa (-ae): extension of a septum beyond the wall; • costa (-ae): a rib or riblike structure; • columella (-ae): central axial structure within a corallite; if present, it can be formed either as a solid columella: a central rod; spongy columella: formed by the inner ends of septa; papillose columella: may small rods; or lamellar columella: plate-like; • dissepiment: horizontal partition (flat or curved) within or outside of a corallite; • synapticulum (-ae): a conical or cylindrical supporting process, as those extending b/w septa in some corals; • coensarc: the living axial part of a coral colony (= peritheca); • peritheca: the living tissue surrounding or between corallites (= coenosarc); • coenenchyme (=coenosarc) the mesogloea surrounding and uniting the polyps in compound anthozoans; • mesentery: a fold of the peritoneum that connects the Fig. 38 coral anatomy (top) vs. coral structure intestine with the posterior abdominal wall. and features (bottom)59 http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 19/70

Corallite growth-form of colony-forming stony corals54: die koralliten-anordnung einer kolonie ist ein wesentliches erkennungsmerkmal zur artunterscheidung;

Fig. 39a plocoid: short Fig. 39b cerioid: corallites Fig. 39d flabelloid: Fig. 39c meandroid: corallites arranged in stalked corallites separated juxtaposed, and are even corallites arranged in single series; by coenosteum while each corallite retains multiple series (due to its own wall; massive corallites in long intra-tentac. Budding); meandering rows or corals that have corallites massive corals with coral valleys that share a sharing common walls mouths aligned in valleys common base, however separated by ridge; the walls (or ridges) of adjacent valleys share the adjacent valleys are not same ridge connected

subplocoid: corallites sometimes separated by coenosteum

Fig. 39f phaceloid: Fig. 39g solitary: Fig. 39h dendroid: the corallites separated by corallum formed by only corallites branch from void space; corals that one individual each other in a dendritic have corallites with pattern; derives from Fig. 39e flabello- distinct walls separated by extra-tentacular budding meandroid: corallites in coenosteum (extinct) long meandering rows with common base; walls may be partially fused. This condition is also referred to as flabellate

Fig. 39i thamnasterioid: Fig. 39j hydnophoroid: Fig. 39k fasciculate: the corallites are cylindrical but the septa of adjacent coral with cone-shaped not in contact. It may be dendroid (with irregular corallites are confluent protuberances between branches) or phaceloid (with more or less subparallel and often twisted or corallites sinuous in form; plating corallites with connecting processes). coral with no walls surrounding corallites

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Colony growth-form of stony corals (scleractinia)55:

Acroporidea growth form: arborescent- colonies typically composed of tree-like branches; bottlebrush - colonies have small branchlets coming out from the sides of the main branch; caespitose - Colonies are "bushy", consisting of possibly fused branches inclined at various angles; corymbose - colonies are composed of horizontal (possibly fused) branches, with short vertical branchlets; digitate - Colonies are composed of short, non-dividing branches, similar to fingers; encrusting - colony adheres to the substrate; flat plates or whorls - plates generally are horizontal, upward facing side with polyps. Whorls tend to be "double-sided" with polyps and are vertical; table - colonies are flat and attached either with a central foot or on one Fig. 40a morphology of a coral side to the substrate; colony53 general coral growth form: massive: mounding, mound-shaped or encrusting colony; similar in all dimensions; branching: colony composed of elongate projections, arborescent, or tree-like to digitate or finger-like platy: laminar, flattened or sheet-like, may be vertical or horizontal colony with calices on only one (monofacial) or both side (bifacial); foliaceous: leaf-like, thin, folded plates or spires extending upward.

Fig. 40b arborescent Fig. 40c bottlebrush Fig. 40e corymbose

Fig. 40d caespitose

Fig. 40f digitate Fig. 40g encrusting Fig. 40i table Fig. 40h flat plates or whorls

Fig. 40j massive Fig. 40k foliaceous Fig. 40l leafy Fig. 40k solitary

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Physiology of scleractinian corals61: alle riffbildenden korallen leben in symbiose mit einzelligen algen (zooxanthellen), die eminent wichtig für die kalkbildung sind. Diese endosymbiontischen algen können, wie jede pflanze, ihre fotosynthese nur bei ausreichend licht durchführen.

Coral-Algae - my best friends are : Symbiosis is the key to understanding ecology of coral reefs and the success of reef-building corals. A. Symbiosis: a close association of two species. 1. Both species live closely together. In some cases one species may live inside another (endosymbiosis - endosymbionts.) 2. No implication of benefit or harm to associates. B. : an association of two species in which each species derives benefit from the association. May be an interdependent association; e.g. = algae + fungi. Reef-building (hermatypic) corals are characterized by presence within their gastrodermal tissues and oral discs of endosymbiotic algae called zooxanthellae. A. Zooxanthellae are minute, spherical unicellular algae belonging to the dinoflagellates. B. Zooxanthellae are acquired during the planula larval stage and proliferate as coral grows. C. If algae are isolated from and cultured, they transform into typical biflagellate, motile dinos. D. Algae can be expelled from host under stressful conditions such as seen in recent coral bleachings, and can be reacquired. E. Means by which corals are “infected” unclear but probably through ingestion, since algae reside in gastrodermis of host. F. Whether >1 species of algae acts as the symbiont to all corals (as well as other hosts) or a single species is not clear, although there is evidence of different genetic strains in different hosts. G. All reef-building corals are zooxanthellate, but not all zooxanthellate corals are reef builders. Non- zooxanthellate corals are not reef builders (ahermatypic). H. Other marine that harbor zooxanthellae: Tridacna (giant ), nudibranchs (Tridachia), Cassiopeia jellyfish, sponges, anemones. Nature of the relationship between zooxanthellae and coral has been a major problem and subject of debate. Alternative hypotheses include the ff. A. Algae are a food source for host. 1. Although corals are known to be micro-carnivores, feeding on zooplankton, this food source may be insufficient to sustain coral growth. 2. Under starvation, corals expel algae and die. 3. Through use of radioisotope 14C, experiments showed that tracer is fixed by zooxanthellae and later dispersed throughout host tissues. In Zooanthus, products of photosynthesis are directly transferred to host (such as glycerol, glucose, alanine). 4. Algae themselves are not digested, but 94-98% of organic carbon produced by algae is utilized by coral host. B. Corals are variably dependent on zooxanthellae. 1. Porter (1976) plotted caribbean coral species on axes of polyp diameter (DP) vs. surface area to volume ratio (AS/V) of live tissue volume of skeleton plus tissue. 2. P is a good measure of zooplankton-catching ability while s?n provides a measure of light-gathering ability. ? 3. Resulting hyperbolic distribution suggests a spectrum of dependence on algae, although even those with low (sn?) input must have some help from algae. 4. Porter found that Montastrea cavernosa obtains only 10-20% of daily energy needs during 2 most successful hours of nocturnal zooplankton feeding. 5. Occurrence of a Porites colony within osculum of a suggests zooplankton feeding is not essential for nutrition (Porter, 1974). C. Zooxanthellae aid in skeletal excretion. 1. Zooxanthellae remove phosphorus as a waste product from coral. Because dissolved phosphate may inhibit calcification, this may benefit growth of coral skeleton. 2. Also remove waste CO2 from coral. D. Zooxanthellae enhance coral calcification. 1. Lab and field experiments of Goreaus using 45Ca showed calcification 2-3x greater in the light. 2. Corals kept in the dark cannot calcify as rapidly and eventually expel zooxanthellae.

3. Photosynthesis reaction: 6CO2 + 6H2O → C6H12O6 + 6O12 + - 4. Hydrocarbonate reaction: CO2 + H2O → H2CO3 → H + HCO3 ++ 5. Calcification reaction: Ca + 2HCO3 = Ca(HCO3)2 ↔ CaCO3↓ + H2O + CO2↑ 6. Removal of CO2 through photosynthesis will enhance calcium carbonate precipitation.

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 22/70

F. Does O2 production by algae benefit coral? Probably not, since reef waters are usually rich in O2. G. Algae benefit in receiving CO2 and other wastes from coral, as well as gaining a living place, almost a “culture medium.” Additional modes of coral nutrition. A. Particle feeding using mucous nets and strings. B. Direct absorption of dissolved organic matter through ectodermis. Für die mechanismen der kalzifikation und carnivore ernährungsweise siehe Velimirov-script2.

Nearly 90% of the carbon fixed by zooxanthellae is released to the coral host primarily as glycerol. Nitrogen and phosphorous derived from captured Fig. 41a Nutritional balance plankton are shared between symbiont and host. The contribution made to the calcification process is of pivotal importance to this discussion. While this link is well known, the precise pathways along which it occurs remain the subject of considerable discussion (Gladfelter, 1985).

Zooxanthellae are unicellular yellow-brown () algae which live symbiotically in the gastrodermis of reef-building corals. It is the nutrients supplied by the zooxanthellae that make it possible for the corals to grow and reproduce quickly enough to create reefs. Zoo- xanthellae provide the corals with food in the form of photosynthetic products. In turn, the coral provides protection and access to light for the zooxanthellae. Because of the need for light, corals containing zooxanthellae only live in ocean waters less than 100 meters deep. They only can live in waters above 20°C and are intol-erant of low salinity and high turbidity. It was once believed that all zooxanthellae were the same species, microadriaticum62. However, zooxanthellae of various corals have been found to belong to at least 10 different algal taxa. Interestingly, zooxanthellae found in closely related coral species are not necessarily closely related themselves, and zooxanthellae found in distantly related coral species may, in fact, be closely related (Rowan and Powers, 1991). This suggests that coral and zooxanthellae evolution did not occur in permanently associated lineages. Rather, symbiotic recombination probably shaped the evolutionary process, allowing both symbionts to evolve separately. Der lichtfaktor verhindert also riffbildung in grossen tiefen und in planktonreichen meeren. Es sind keine zooxanthellate riffe gefunden worden, die tiefer als 100m unter der meeres- oberfläche sind. Die korallenfärbung ist durch die eingelagerten zooxanthellaten verursacht (protisten aus der gruppe der dinoflagellaten der gattungen Gymnodium = Symbiodinium), z.b. S.microadriaticum. Im allgemeinen fall wird die alge mit der planula larve weitergegeben, sodass die jungkoralle schon nach der Fig. 41b Gymnodium metamorfose mit dem aufbau einer kolonie beginnen kann. microadriaticum Im zuge einer korallenbleiche gehen viele zooxanthellen durch exocytose verloren; ist die zeitdauer der externen stress-einwirkung zu gross werden dass selbst die noch wenigen verbliebenen endosymbionten exocystieren, so kann die koralle selbst nach ende der stress-einwirkung keine neuen zooxanthellen kultivieren und geht letztendlich kaputt. Korallenkolonien die in lagunen gedeihen sind auf einen ausreichenden wasser-austausch angewiesen um ein exocystieren der endosymbionten zu vermeiden; oft verhindert die wasser-luft grenze ein weiterwachsen nach oben, wodurch der stock apikal abstirbt (UV-einwirkung und längeres trockenfallen lösen exocytose aus), kann allerdings durch laterales wachstum eine mikroatoll-struktur annehmen (koloniezentrum erfährt vertiefung, ist bei Porites-kolonien häufig zu beobachten).

Fig. 41c SEM of zooxanthellae.

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 23/70

PART III - Reef zonation64:

There are four basic types of coral reefs; fringing, barrier, platform, and (for details see Velimirov- script2): • Fringing reefs are located very close to shore, and because of water run off they are typically high in nutrients and the water has a high turbidity. • Barrier reefs are further from the shore, with a "lagoon" between the reef and the shore. • Platform reefs are formed in midocean locations, and at the edges of continental shelfs. • And finally are a circular reef with a central lagoon and possibly small islands formed on the reef. It is theorised that each of these types of reefs corresponds to a differing age of the entire reef structure. The youngest is the , with the corals colonizing a shallow water area close to the land. If the sea levels then rise or the land subsides, then the reef structure keeps up with this changing depth by growing upward. Eventually a shallow area with no coral growth will form behind the main reef, called a lagoon, giving a barrier reef. If the sea level or land subsides so much as to cause the land to disappear below the water surface, then an atoll is formed. The overall type of the reef whether it is a turbid, high nutrient reef where the stony corals are less common and algae abounds or crystal clear, low nutrient reef where the stony corals can dominate, is dependent of several factors. These include the proximity to land (therefore water run off which will be high in nutrients), proximity to river mouths (for the same reason as land proximity), and location of deep sea currents (which typically bring nutrient rich water. Each type of reef is also divided into various zones within each reef.

Fig. 42a Coral Reef distribution and diversity: coral reef development is restricted to the low-latitude area between the two 18°C temperature lines shown on the map. Minimum water temperatures of 18°C in surface waters of the Northern and Southern hemispheres occur in February and August, respectively. In each ocean basin, the coral reef belt is wider and the diversity of coral genera is greater on the western side of the ocean basins (after Stehli and Wells, 1971).

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What is coral reef zonation? Zonation is a very important concept when considering any ecosystem, with coral reefs being no exception. A particular ecosystem will typically be divided into zones, each zone having a particular set of physical parameters, such as light intensity, that set it aside from any other part of the ecosystem. A zone is defined by its physical parameters and location within the ecosystem. Within a particular zone, various organisms will have evolved such that they are adapted to thrive under those specific conditions that are present within that zone. It can undoubtedly live somewhere else, in a similar zone or sometimes even one vastly different, but there is always one in which it will be perfectly suited and as a result outcompete any other organisms that occupies that niche in the food web.

What determines coral reef zonation? Zonation within a reef is typically determined by: a) the light intensity received, which is dependent of the depth and turbidity of the water; b) position relative to the open ocean or river mouths; c) deep ocean currents; and d) localized water currents. Each of these parameters interact to give the final conditions that are characteristic of that zone. The most dominant parameter is the light intensity, which is the major source of energy for the reef community. And because this is directly related to the depth; depth can be used as a very good indicator of the predominant conditions. As a general rule with increasing water depth: • light intensity drops; • blue light increasingly becomes the more dominant wavelengths in the light spectrum, as the other wavelengths are absorbed more rapidly by the water; • wave surges become less intense, but currents can still remain strong; • water temperature falls and becomes more constant (a reason why bleaching usually takes place within the first 10-15m depth range).

Therefore the particular organisms that are present on the reef alter with the depth, as each one has evolved to fit best into one area. The organism can also alter its behavior depending on the zone, with the physical conditions having a large effect on its behavior and even its appearance. This is graphically shown by many of the stony corals. In the shallow, high light intensity and extreme water motion zones they will form fingered or massive (domed) structures. As the depth increases, light intensity rapidly drops off and wave surges are reduced, but the currents can still remain strong. To adapt to this lower availability of light, stony corals then take on thin, flattened plates therefore increasing the surface area that is exposed to light. Storms are another factor that can also affect and alter the zonation of a reef. Fig. 42b Reef Zonation The force of the waves and associated surges batter the reef structure, break some of the reef building corals weakened by boring organisms, distribute erodied sediments, and erode the shores of coral cays.

Deep Forereef: the forereef slope is the least consistent of any of the reef zones, in either its occurrence or character. At many sites, it is totally absent and the forereef drops from shallow water to oceanic depths. Where a forereef slope is present, the deep forereef usually occurs as a well-defined ridge near the platform margin. Otherwise, it is simply a down-dip extension of the forereef. When occurring separate from the shallower reef zones, the location of the deep forereef is probably controlled by both the break in slope and the existence of an antecedent high left by a previous reef. The character of the reef surface is often similar to the spur-and-groove topography described within the forereef section, except that the scale of both the reef promontories and the intervening channels is generally larger. The Deep Fore Reef Slope (50 - 300m deep), represents the seaward limit of the reef. Typically, this boundary is a steep underwater cliff (often referred to as “the Wall”) where organisms cling to irregular rocky

ledges. As sunlight gradually disappears, the reef biota give way to a Fig. 43a Deep Forereef community of sponges and deep-water, non-reef-building corals. http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htm Antonius 25/70

In this image, note the steep slope (about 70o) of the reef rising. Perhaps the most dramatic feature of the deep forereef is the “reef wall”. At depths ranging from 50 to 85m around the Caribbean, the forereef slope rolls over to a vertical or, in some places, overhanging precipice. The role of active accretion at this depth is not well understood, owing to its remoteness. Along the high- energy margin of the Great Barrier Reef, coral cover is apparently limited to a very thin Fig. 43b Coral gradient veneer over the antecedent Pleistocene reef front (Isdale, 1984). Along the front of the barrier reef, several episodes of reefwall accretion have probably occurred (James & Ginsburg, 1979).Compression of the coral; reef zonation is accompanied by some changes in the coral community, with the less sediment-tolerant (Montastraea annularis, and Acropora palmata) being reduced in present of total cover.

Reef Slope: below 20m in depth on the reef front is the reef slope – the reef has extended into deeper offshore waters. Because of the increased depth, sunlight is not as intense. In response to lowered light levels, corals adapt and grow as large plates. Some of the plates seen here are species which form rounded heads in shallow water. At these levels the blue part of the light spectrum dominates and the light available is vastly lower than that at the surface. Corals expand horizontally in shape in order to capture as much sunlight as possible. Therefore any branching species that are found in shallower waters are largely replaced by plate-like forms of the same species. Gorgonian fans (Gorgonacea) are very prolific in this zone, along with the feather stars (Crinoidea) that are associated with gorgonians. The dominant genera present are: Scleractinians: Echinopora, Porites, Turbinaria, and Acropora. (indo-pacific only: A.hyacinthus, A.clathrata, A.cytherea) Alcyonaceans: Dedronephthya. Gorgonacea: etc. Tridacnidae: Tridacna gigas (indo-pacific only) Cypraeidae: Cypris sp. Fig. 44 Reef Slope Pisces: , Chaetodontidae, Ephippidae, Mobulidae, etc,

Reef Terrace: as the name implies, the Reef Terrace is a relatively flat surface of the reef which extends from 10-15m water depths offshore of the reef crest. In the Caribbean, this environment is dominated by the slim branching coral, Acropora cervicornis, with interspersed larger head corals of Montastrea species. In this view, the thin sticks on the bottom are remains of A. cervicornis, which was devastated by Hurricane Allen in 1980. Fig. 45 Reef Terrace Reef Front / Forereef Front / Buttress Zone: the reef front may be the next part of the reef as land is approached, i.e. front of the forereef. As the sea floor starts to approach the surface, then enough light starts to penetrate and supply the energy required for a reef community to exist. This is divided into two sub–zones, the reef slope and upper reef slope. The Buttress Zone is a portion of the reef where environmental conditions are optimal for growth of many reef organisms (5 - 10m deep). The result of this ideal environment is the development of large coral buttresses which extent seaward and rise Fig. 46 Buttress zone above sand channels. Because this setting is so ideal for reef biota, it is characterized by the highest diversity of any sites on the reef. The dominant genera present are: Scleractinians (indo-pacific: Platygyra sp.; altlanic: Diploria sp.). Pisces: Balistidae, , Acanthuridae, Labridae, etc.

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Fore Reef (Upper Reef Slope / Seaward Platform): the forereef extends seaward and downward from the reef crest. It is the most complex of the reef zones, owing to the large depth gradient over which it occurs. In many areas, the forereef is organized into a set of en-echelon reef promontories and sand channels, termed “spur-and-groove” topography, with fingers of coral formations penetrating into the ocean with channels in-between. Spur-and-groove is common in both modern and ancient reefs. The term was originally Fig. 47a Fore Reef coined from Indo-Pacific examples formed by erosion of the algal rim just below the surf zone. More recently, examples have been described from the Caribbean that appear to be the result of accretion by Acropora palmata under the influence of strong wave surge. Both the coral branches and the intervening sand channels are oriented parallel to the dominant wave-approach direction (Shinn, 1963; Roberts, 1974). Hubbard, et al. (1974) proposed that the channels serve as primary conduits for sediment export from the reef. They further proposed that spur-and-groove topography will be best- Fig. 47b Acropora palmata developed along windward margins where a barrier exists to bankward transport, and downslope sediment movement is the only means of export. The spurs are typically dominated by large fingered structures of Acropora and massive coral species. The spur formations provide calmer regions where fleshy green algae, sponges and encrusting corals can grow. The sandy groove regions support little coral or algae growth because of the strong scouring surges and tidal run-off running through these grooves. But tough algae such as Halimeda can survive. The grooves often open out to a region of rubble and coarse sand. This entire zone provides a region where nutrients are concentrated then transported into the reef flat area by algae growing then becoming detached. The Barren Zone is another rigorous, wave swept environment, but it forms immediately seaward of the reef crest. Large blocks of coral are also toppled and pile against the reef edifice during storms. There are many fewer soft, fleshy algae in this setting because fish and other grazers of the reef gobble them up. Corals have to take on expansive body forms designed to maximize the exposure to sunlight, but are not limited to the vast horizontal plates characteristic of the reef front. The shallower Fig. 47b Spur and groove system of the fore reef regions also have more Scleractinians because of their more robust structure, higher growth rates under intense light and territorial defense mechanisms. Feather stars, sponges and other suspension feeders expose themselves to intertidal currents on structures that jut out into the currents, such as gorgonians. Inside overhangs and caverns, azooxanthellae corals, sponges and soft corals are dominant. The dominant genera present are: Alcyonaceans: Lemnalia, Lobophytum, Nephthea, Sarcophyton, Sinularia, and Xenia. Scleractinians: Acropora, , Favia, Favites, Leptoseria, Lobophyllia, Plerogyra, , Porites, Millepora, and Stylophora. Zoanthidea: Palythoa. Pisces: Scorpenidae, Pomacanthidae, Labridae, Acanthuridae, etc.

Reef Crest (Reef Rock Rim): the crest of the main reef is generally emergent in Pacific reefs at low tide, but may be below the surface in Caribbean reefs. The seaward edge of the reef crest takes the brunt of the incoming wave energy. Attenuation of wave energy by the reef crest. Roberts (1989) has shown that the reef can reduce incoming wave energy by up to 97%. As waves break, water is washed across the reef crest and into the lagoon, driving lagoonal circulation (Hubbard, et al., 1981). One of the services provided by reefs is a regeneration breakwater protecting coastal areas. The change in wave energy results in a different physical regime leeward of the crest than the reef front. It is the highest energy zone of a coral reef ecosystem, with very intense light, and intense wave action and surges. Fig. 48a Reef Crest

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Corals that live within this zone are typically very short and fingered or massive in structure to withstand the strong wave action and as such don’t have to spread out to capture light. Almost all surfaces in this zone are exposed to some light (not just the upper area as in the deeper reef front zone) so the massive and fingered structures utilized this fact and are strong enough to resist the strong currents. Furthermore, coralline algae cement this region together, forming a solid terraced like pavement. Fig. 48b Reef Crest Often, sand binding algae mats that entrap sediment. The dominant genera present are: Alcyonaceans: Lobophytum, Sarcophyton, and Sinularia. Scleractinians: Acropora, Favites, Montipora and Pocillopora. (Dioploria clivosa in atlantic reefs, while Leptoria phrygia is dominant in indo-pacific reefs) Zoanthidea: Palythoa.

Reef Flat: because of the modification of wave forces across the reef crest, the backreef is an environment of totally different physical processes, ecology and sediment characteristics. Sediments and rubble from the reef crest are dumped behind the crest, widening the backreef flat through time. The outer reefs of the Great Barrier Reef have been at sea level for nearly 6,000 years. Hence, the wide backreef flats often exhibit distinctive front-to-back zonation. By comparison, Caribbean Fig. 49a Rear Zone reef flats have only recently reached sea level and are narrower. The

organisms of the reef flat must be able to withstand intense ultra violet radiation, desiccation, high salinities and elevated water temperature. This zone is divided into two sub-zones, living coral sub zone and sand sub-zone. Coral cover decreases inward, with sand covering the inner part of the reef flat. While zonation is less pronounced, there is a general transition from branching corals () and the hydrozoan Millepora near the front of the crest to sand flats and landward. Amongst scleractinians, it may have a shallow Porites reef flat immediately behind the crest and numerous small patch reefs in a sand apron. The corals are generally well adapted to the high levels Fig. 49a Patch reef of sedimentation to which they are regularly subjected. In the Caribbean, the dominant genera include the following Scleractinians: and several other head corals, especially Montastrea annularis, Porites asteroides and species of Diploria. This entire zone is usually most prolific with Acropora, Actiniarians (anemones), Asteroids (), Holothurioids (sea cucumbers), Alcyonaceans, and reef fishes. The Rear Zone is a rigorous, wave swept environment which forms immediately shoreward of the reef crest. Large blocks of coral are transported to the Rear Zone during storms where they will be colonized by dense growths of algae. Few other organisms call this part of the reef home.

Living Coral Sub-Zone: within the living coral sub-zone tongues of the reef structure penetrate into the lagoon with narrow sand channels in- between. This is very similar to the upper reef slope. The coral sand that is present is produced from coralline algae, foraminifers, calcareous algae, and the breakdown of the reef structure. Fig. 50 Channel system Domiant genera of this zone are found among Echinodermata: echinoids (sea urchins), asteroids (starfish), holothurioids (sea cucumbers) and molluscs. Scleractinians: Acropora, Pocillopora, Gonipora, Platygyra, Seriatopora, Lobophyllia, Tubipora, Montipora, Fungia, Goniastrea, Favia, Favites, and Porites. Pisces: Fistulridae, Serranidae, etc.

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Sand Sub-Zone / Lagoon: reef-building corals often build upward very close to sea-level. As such, they frequently cause water to be impounded in a shallow basin between the shore and the reef crest. This is called the Lagoon Zone, and it is an environment separate from but still part of the reef system. Lagoon waters may vary greatly in salinity, temperature and turbidity. This environment is home to a large community of algae. Gradually the reef structure gives way to vast areas of coral sand eroded from the main reef structure. Dotted throughout this zone are small ‘islands’ of Scleractinians that rise up Fig. 51 Lagoon out of the sand. In the calmer regions delicate branched corals form intricate growths. The lagoon is constantly supplied with nutrients and sediment removed from the reef front and reef rock rim zones, with some becoming muddy from the accumulated sediment. Seagrass beds grow on shallow lagoon floors and reef flats and are also very important for coral reef ecosystems. They act as nurseries for the young of many coral reef fishes. Seagrasses also trap sediment in their roots, preventing cloudy water from settling on nearby coral reefs. Holothurioids are prolific inhabitants and constantly rework the surface sediment. Deeper lagoons with heavy sediments or high turbidity have: Scleractinians: Cataphyllia, , Gonipora, Leptoseris, Pachyseris, and Montipora. The island or patch reefs that rise out of the lagoon floor consist of: Scleractinians: Acropora, Favia, Favites, , Goniastraea, , Pocillopora, Porites, Seriatopora, Stylophora, and Tubipora. Spread over the sandy bottom can be found: Scleractinians: Heliofungia, Fungia, and Herpolitha. Other families present: Alcyonaceans: Heliopora, Sarcophyton, Lobophytum, Xenia, Cespitularia, and Sinularia. Coralliomorpharia: Rhodactis. Zoanthidea: Palythoa, and Zoanthus.

Cay – : this is another high energy zone, with the organisms that live here adapted to withstand intense ultra violet radiation, desiccation and high salinities. There is usually water retained in tidal pools even at low tide. Some corals can survive this harsh environment completely exposed to the air. Coral cays are formed when broken down fragments of corals and algae wash onto the Fig. 52 Michelmas cay (north shallow top of a coral reef. If enough of the sand and rubble collects, QLD - AUS) a small island or cay is formed. The exposed areas are homes for birds and nesting sites for turtles. Gastropods are very common in this zone, and usually the most conspicuous inhabitants. But there is also a multitude of interstitial sand fauna that extensively inhabits this zone. Specific family information has yet to be found.

Shore Zone – Beach: finally then comes the beach. Any thing inhabiting this region is very resilient. Some obvious organisms are molluscs (mainly that bury themselves in the sand) and decapods (crabs). The shore zone marks the boundary between terrestrial and marine environments. In many tropical localities worldwide, this zone is occupied by dense tangles of mangrove trees. The mangrove is a very hearty bush which can tolerate salt water. The numerous prop roots provide habitat for a great diversity of algae, sponges, Fig. 53 Shore marine invertebrates. They also act as nurseries for young shrimp and fishes, including many species of coral reef fishes. Their falling leaves also provide fish with food and important nutrients. One of the most important functions of mangroves is that they filter the mud and sediment between the land and the coral reef. When a mangrove forest is cut down, the mud, silt and fresh water can leak out to the coral reef, which can smother and kill the corals. Sandy Beaches with trees and plants can also be extremely important for the health of coral reefs. Similar to the mangroves and seagrasses, the sand acts to filter sediment from the land, preventing it from smothering the reefs. When sandy beaches and plants are removed, sediment from storms can run straight into the ocean and onto the coral reefs.

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Reef Communities:

Reef Dwellers and Infillers: major proportion of reef mass is contributed by plants and animals inhabiting the framework. A. Framework not only provides living space for organisms but also traps their shells and skeletons. B. Many reef dwellers enhance trapping action of reef through sediment baffling and binding. C. Sediment contributed by various dwellers is highly variable in size, shape, mineralogy. Algae A. Four major groups: blue-green, green, brown, red. B. All present on reefs. C. Calcification occurs mostly in greens and red algae, but even non-calcareous forms act to trap and bind sediment. • Green algae (Chlorophyta): major producers of sand, silt, mud; e.g. Halimeda. Penicillus. Udotea. • Brown algae (Phaeophyta): only Padina calcifies. • Red algae (Rhodophyta): major role as cementers, e.g. Porolithon, Melobesia; also form sediment (Goniolithon). • Blue-Green algae (Cyanophyta): trap and bind sediments to form stromatolites in back reef areas, lagoons, tidal channels. Higher plants: turtle grass (Thalassia) forms extensive meadows in back reef, lagoons, and mangroves along sandy, muddy shores. A. Dense root mat binds sediment. B. Blades trap fine carbonate on sticky surface, baffle other sediments. Animals A. Protozoa: foraminifera are important contributors. B. Porifera: sponges contribute spicules, chips from excavation of clionids. C. Coelenterata: Alcyonarian spicules. D. Mollusca: major contributors to reef debris: gastropods, bivalves, . E. : crabs, lobsters, barnacles, ostracods contribute calcareous skeletal material. F. : crinoids, brittle stars, sea stars, echinoids, cucumbers all contribute skeletal debris. G. Pisces: contribute to ultrafine coral sediments, while other herboivores such as damlsefish, doctorfish, etc. control the algal populationn on the reef.

http://www.sbg.ac.at/ipk/avstudio/pierofun/funpage.htmFig. 54 Reef organisms

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The Role of in Coral Reef Ecology68: coral reefs depend heavily on bacteria in all manner of action. The majority of bacteria in the water column are free living and feed on dissolved organic matter. These microbes will process the organic matter in the water with a 30-50% efficiency rate. Pelagic bacteria can double their populations within one tide change to respond to an increase in nutrient levels. Bacteria normally compose between 5 and 20% of the total biomass of plankton, either free living in the water column, or associated with particulate matter. This number represents an even larger planktonic mass than zooplankton. They are also responsible for up to 30% of the primary production of reefs.

Fig. 55 Microbial food web (left), conventional food chain (right)

The “microbial loop” in the waters above and around a coral reef revolves around bacteria, organic matter, and the bacteriovores (zooplankton) such as foraminifers, acantharians, radioarians, copepods, etc.). This micro-food web is not only important in and of itself, but is also crucial in the maintenance of the phytoplankton populations as it is a major provider of N- and P- compounds. Because of the productivity of the reef organisms, there is a level of microbial substrate produced by the flora and fauna that allows for bacterial productivity in the water column above the reef to be magnitudes of order above that in oceanic waters. As such, they may be responsible for 40% of picoplankton production and 25% of microplankton production. In other words, even in the water column, bacteria are the beginning and end of the plankton that feeds the coral Fig. 56b Foraminifers reef. The bacterial aggregates associated with particulate matter (detritus, phytoplankton debris, mucus, etc.) comprise only about 25% of the total bacterioplankton. Still, they enrich the particulate matter with their mass (termed “reef snow,” or” marine snow”), becoming a very important nutrient source for coral reef filter feeders and planktivores. The important nutrient cycle that centers around particulate matter and bacteria is termed the “detrital web” (the nutritional aspect of bacteria to corals will be covered later). Fig. 56c Acantharians

Fig. 56a Eubacteria (left) cyanobakteria (right)

If anyone thought that the importance of bacteria in the water was impressive, it is nothing short of trival compared to what happens in Fig. 56d Radiolarias the sediments. If the aggregates of bacteria and suspended particulate matter are not consumed, they have a great chance of settling out on the sediments of the reef and the lagoon. Much of the waste material, algae debris, mucus and excess production from the reef is also drawn towards shore, where it settles on the soft bottoms.

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There, it fuels the growth of a diverse community of bacteria, detritivores, and other planctonic flora and fauna. They mediate the return of organic and inorganic matter back into the food web, provide for the decomposition of waste and decaying and animal matter, and allow for the beginning of new productivity by providing food and nutrients to algae and microfauna. Frequently, sea grass beds are found in areas of heavy organic enrichment. These true plants (not algae) are associated with some of the most highly productive communities on earth. In and around their root structure, microbial production is as great as in any sedimentary community known. Even the productivity and decompostion abilities of the terrestrially enriched mangroves owe their effectiveness to bacteria and the community they sponsor. Perhaps surprisingly, mangroves are typically sources of limiting organic matter which are exported to the reef, rather than being consumers of it. Lagoons and sea grass beds depend heavily on the organic matter produced by the reef, where the productivity of the bacterial community, by some estimates, equals or exceeds the gross productivity of the entire reef itself! The upper one centimeter of lagoon sediments contain as much microbial protozoic microfauna biomass as all the water column above it. To further emphasize the immense capabilities of these areas, they are actually nutrient limited! Here, bacteria are intricately interwoven in the carbon cycle, the phosphorous cycle, and the nitrogen cycle. Most of the material Fig. 57a Phytoplankton exported from the reef is either utilized by the lagoon benthic communities for their own sustenance, or put back into the food web after decomposition, remineralization and processing. It then serves as a food material for the various , sponges, ascidians, corals, bivalves, and plankton that inhabit the reef. A relatively small portion is either lost to the atmosphere or washed back into oceanic regions. However, the ultimate regeneration of nutrients is in their uptake into the reef community for growth and reproduction, They may also be indirectly incorporated into the nearly permanent reef structure itself by sustaining the metabolism of Fig. 57b Zooplankton the hermatypic corals.

In summary, bacterial action and productivity is absolutely essential to the reef environment, and provides, arguably, the largest role in its success. Still, the primary nutrient which limits the bacterial populations is carbon. Adequate sources of carbon are largely provided by the success of the coral community. Once again, these two groups are wholly dependent on each other, and are inextricably woven together. The denser the coral growth, the more abundant the microbial growth. The denser the microbial growth, the more Fig. 57c Nekton abundant the corals.

Fig. 57d Trophic levels

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Algal communities on the reef65: algae comprise a grouping of very diverse photosynthetic organisms whose relatively simple vegetative structure is called “thallus”. They are distributed in several lineages (divisions) which have evolved independently from each other. In simple terms, we identify a “red lineage” with the red algae or Rhodophyta, a “brown lineage “ with in particular brown algae or Fucuphyceae, and a “green lineage” grouping together “green algae” or Chlorophyta, mosses (Bryophyta), ferns (Pteridophyta), gymnosperms (Pinophyta) and flowering plants (Magnoliophyta). As for blue-green algae, they are grouped with bacteria and are known as Cyanobacteria. Algae are autotrophic organisms, which are able to manufacture their own organic molecules from elements containing carbon and nitrogen. Their energy is obtained from sunlight, which is trapped by the chlorophyll pigment. Furthermore, certain algae such as Ulva, are capable of directly incorporating organic substances, while the unicellular algae euglenoids and dinoflagellates capture, phagocytose and digest their prey. They are basically aquatic organisms, even if some (like the green algae Rhizoclonium) temporarily colonize exposed habitats.

Division Chlorophyta or green algae: chlorophyta are algae whose thallus is typically green in color due to chlorophyll a and b pigments that are dominant in the chloroplasts. However, prolonged exposure to strong light leads to the synthesis of photoprotecting pigments (carotenoids) that turns the thalli orange to yellow. This group of algae which is poorly diversified in temperate waters is in fact rich in species and forms in tropical waters. Green algae are present in all aquatic systems, from marine to freshwater habitats. The most diversified Chlorophyta are Caulerpa and Halimeda. The Fig. 58 Caulerpa bikinensis cosmopolitan Ulva and Enteromorpha species abundant in calm (occasionally eutropicated) waters with variable salinity. However, Ulva blooms remain relatively infrequent on reefs compared to the "green tides" that they create in several areas of the world. In French and in the Cook Islands, the Boodlea kaeneana algae can, on certain reefs and in the lagoons, bloom in spectacular fashion during the southern summer. An overcharge in nutrients linked to growing urbanization, in addition to strong sunlight, is the most probable hypothesis to explain this proliferation.

Division Phaeophyta (Chromophyta) - Fucophyceae or brown algae: within the Chromophyta, brown algae are grouped in the Fucophyceae class, formerly called Phaeophyceae. These are almost exclusively marine algae. Their color is due to the abundance of brown fucoxanthin pigments that mask chlorophyll a and c. Fucophyceae display great morphological diversity, from relatively simple filamentous forms to the large brown algae (Turbinaria, Sargassum) whose complex morphology approaches the leafy stems of higher plants. Brown algae are mainly diversified in cold and Fig. 59 Lobophora variegata temperate seas where they form large underwater forests (kelp forests). In tropical waters they represent fewer species, but have the largest thalli and form the densest populations.

Division Rhodophyta or red algae: rhodophyta are the most numerous algal group in tropical regions. They show a particular originality with their dominant red (phycoerythrins) and blue (phycocyanins) pigments that mask chlorophyll. The relative proportions of the different pigments, in conjunction with the shape of the thallus, result in a range of all imaginable colors from dark brown to light pink, purple reds and orange tints. Furthermore, within a single species, color varies according to the exposure to light and often individuals that grow in strong light display faded colors where orange-yellow Fig. 60 Galaxaura fasciculata hues dominate due to the strong concentration of photoprotectant carotenoid pigments.

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Kingdom Bacteria phylum Cyanobacteria (blue-green algae, Cyanophyceae, = Cyanobacteria), being autotrophic (actively utilize sunlight and CO2 to meet their energetic requirements) fundamentally differ from other groups of algae, since they are categorised as bacteria. They belong to the most ancient forms of life on Earth. During the era (about 1.5 billion years ago), they built- up rocky formations called stromatoliths, either by the precipitation of calcium or by the trapping of sediments. Despite their very ancient origin, we should not consider them as a relic group, on the contrary, Fig. 61 Phormidium sp. though discrete, they occupy all types of habitats, even those inacces- sible to other organisms. They are generally microscopic filamentous forms that bore into calcareous substrata, or adhere to each other to create colonies of strongly variable sizes, shapes and colors. Like red algae, they possess more blue (phycocyanin) and red (phycoerythrin) pigments that mask chlorophyll a. Despite their former name of blue-green algae, they are rarely blue but more often red, green with blue, violet, brown, yellow or orange hues. Most of them have a gelatinous or even sticky texture, owing to mucilaginous secretions, but this is not generally the rule. In addition to their photosynthetic ability, Cyanobacteria play an important role in the biosphere by transforming atmospheric nitrogen into nitrates which are directly used by other organisms. This ability is of fundamental importance on coral reefs, where nutrients are scarce. Furthermore, Cyanobacteria are for humans choice microorganisms in several branches of biotechnology, owing to the numerous families of chemical molecules that they manufacture, which have a potential value. Despite an apparent simplicity in the organization of forms, the taxonomic identification of Cyanobacteria currently remains difficult and complex.

Division Antophyta: the flowering plants; subdivision: Angiospermae, class Monocotyledoneae, subclass Alismatidae (Heliobiae); order Hydrocharitaceae (Thalassia sp, turtle grass) is quite common in the shallow, sandy areas just offshore. As its name suggests, turtles graze on Thalassia and can crop it quite close, sort of like goats grazing a field of grass (the local Exxon company actually uses goats to “mow” their grass). These fields (we call them beds for some reason) of grass are also habitats for young fish and invertebrates and so are considered nursery grounds for the reef and offshore fishery. The blades of Thalassia are long and strap-like, about 1 cm wide, and can grow rapidly in length. These plants are Angiosperms, or true flowering plants. This is in contrast to the other simple reef plants mentioned above. In addition to flowers, Thalassia (as well as our other common Angiosperm Syringodium or Manatee Grass) have true roots and a vascular system for conducting fluids and metabolic signals such as hormones around its body. The roots of Thalassia Fig. 62 Thalassia sp. grow quite dense with 0.5cm thick individual roots matted together to the nearly complete exclusion of the sand!

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Fauna of reefs - invertebrates (the families listed in the following pages represent only some of the sheer endless diversity found in coral reefs, and therefore should not be considered as a comprehensive summary).

Other characteristics of sponges include a system of pores (also called ostia) and canals, through which water passes. Water movement is driven by the beating of flagellae, which are located on specialized cells called choanocytes (collar cells). Sponges are either radially symmetrical or asymmetrical. They are supported by a skeleton made up of a collagen and spicules, which may be calcareous or siliceous, depending on the group of sponges examined. Skeletal elements, choanocytes, and other cells are imbedded in a gelatinous matrix called mesoglea (Gk. mesos, middle; glia, gleu; =mesohyl). Sponges capture food (detritus particles, plankton, bacteria) that is brought close by water currents created by the Fig. 63 sponge anatomy choanocytes. Food items are taken into individual cells by phagocytosis, and digestion occurs within individual cells. Reproduction by sponges is by both sexual and asexual means. Asexual reproduction is by means of external buds. Some species also form internal buds, called gemmules, which can survive extremely unfavorable conditions that cause the rest of the sponge to die. Sexual reproduction takes place in the mesoglea. Male gametes are released into the water by a sponge and taken into the pore systems of its neighbors in the same way as food items. Spermatozoa are “captured” by collar cells, which then lose their collars and transform into specialized, amoeba-like cells that carry the spermatozoa to the eggs. Some sponges are monoecious (individuals produce both male and female gametes); others are dioecious (sexes are separate). In most sponges for which developmental patterns are known, the fertilized egg develops into a blastula, which is released into the water (in some species, release takes place right after fertilization; in others, it is delayed and some development takes place within the parent). The larvae may settle directly and transform into adult sponges, or they may be planktonic for a time. Adult sponges are always sessile. Sponges fall into three main groups according to how their bodies are organized. The simplest sponges are the asconoid sponges. These are shaped like a simple tube perforated by pores. The open internal part of the tube is called the spongocoel; it contains the collar cells. There is a single opening to the outside, the osculum into which all pores converge once the water has been filtered through the collar cells. The osculum is thus the main outstreaming opening of a sponge. The next-most complicated group is the syconoids. These tend to be larger than asconoids. They also have a tubular body with a single osculum, but their body wall is thicker and the pores that penetrate it are longer, forming a system of simple canals. These canals are lined by collar cells, the flagellae of which move water from the outside, into the spongocoel and out the osculum. The third category of body organization is leuconoid. These are the largest and most complex sponges. These sponges are made up of masses of tissue penetrated by numerous canals. Canals lead to numerous small chambers lined with flagellated cells. Water moves through the canals, into these chambers, and out via a central canal and osculum.

Fig. 64 asconoid, syconoid, leuconoid sponges

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Sponges are found in virtually all aquatic habitats, although they are most common and diverse in the marine environment. Many species contain toxic substances, probably to discourage predators. Certain other marine animals take advantage of this characteristic of sponges by placing adult sponges on their bodies, where the sponges attach and grow. The chemicals also probably play a role in competition among sponges and other organisms, as they are released by sponges to insure themselves space in the marine ecosystem. Some of these chemicals have been found to have beneficial pharmaceutical effects for humans, including compounds with respiratory, cardiovascular, gastrointestinal, anti-inflammatory, antitumor, and antibiotic properties. Sponges also provide a home for a number of small marine plants, which live in and around their pore systems. Symbiotic relationships with bacteria and algae have also been reported, in which the sponge provides its symbiont with support and protection and the symbiont provides the sponge with food. Some sponges (boring sponges) excavate the surface of corals and molluscs, sometimes causing significant degradation of reefs and death of the mollusc. The corals or molluscs are not eaten; rather, the sponge is probably seeking protection by chemically excavating into the hard structures it erodes. Even this process has some beneficial effects, in that it is an important part of the process by which calcium is recycled.

Class Calcarea (L. calcarea, limestone) the calcareous sponges; these are the sponges with calcareous (rather than siliceous) skeletons. Their spicules are made up of calcium carbonate; they are simple in structure or may have up to four rays. Members of the Class Calcarea are small. Most are tubular or vase-shaped, and they can have asconoid, syconoid, or leuconoid organizations. All species are marine.

Fig. 65 Leucosolenia sp.

Class Demospongiae (Gk. demos, bond; spongos, sponge): this group include both fresh water and marine species. Their spicules are siliceous but not six-rayed, but the spicules in some forms are partly or completely replaced by skeletal elements made of spongin (a sponge protein). The canal systems are leuconoid. Demospongiae includes a large number of species.

Fig. 66 Spongia officinalis

Class Hexactinellida (Gk. hexa, six; aktinos, ray) the 6-rayed sponges; the Hexactinellida are the glass sponges, so-called due to their siliceous skeletons. The spicules have six rays and are united to form a network. The body is usually cylindirical or funnel-shaped. Most Hexactinellida are syconoid or leuconoid in body organization. All species are marine and most inhabit deep water.

Fig. 67 Aphrocallistes vastus

Class Sclerospongiae (Gk. scleros, hard; spongos, sponge) these sponges are sometimes included in the class Demospongiae. They have a massive calcareous basal skeleton, with the living tissue mostly within the skeleton (extending outward very slightly). These sponges have siliceous spicules and spongin fibers like those of the Demospongiae. Their body plan is leuconoid. They are found in marine environments, usually in association with coral reefs. Notorious for their biodegradive capabilities are sponges of the genera Cliona, Anthosigmella, and Spheciospongia, of the order Hadromerida, and Siphonodictyon (order Haplosclerida). These sponges actively bore into the calcareous substrate of both limestone Fig. 68 Sclerospongia sp.

substrata and precipitated CaCO3 of scleractinian corals.

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Phylum Mollusca73: the name Mollusca (from the Latin mollis meaning soft), was first used by the French zoologist Cuvier in 1798 to describe and , animals whose shell is reduced and internal, or entirely absent. It was only later that the true affinities between these species and other molluscs, such as and bivalves, were fully recognized. The molluscs are a very successful group. If success is measured in terms of number of species and variety of habitats to which they have become adapted, then molluscs are one of the three most successful groups in the animal . Over 160,000 species have been described, of which around 128,000 are living and about 35,000 are recorded as species. Molluscs are found in nearly all habitats. In the sea they occur from the deepest ocean trenches to the intertidal zone. They may be found in freshwater as well as on land where they occupy a wide range of habitats. Thus, during their evolution, they have become adapted to living in nearly all available habitats. The phylum Mollusca is normally divided into 8 orders of very unequal importance; the most important class of living molluscs is the comprising more than 80% of all living mollusc species. Although the Cephalopoda still contains a number of living species, fossil evidence suggests that they were once far more abundant than they are today.

Class Polyplacophora (Gk. poly, many; plax, plate; pherein, to bear) - order , family : the shell is composed of eight overlapping plates or valves. These are joined to each other on the outer margin and undersides to the girdle, a thickened part of the mantle. Scales, spines or bristles may be present on the girdle. Since the plates allow flexibility, the animal is able to mold itself to uneven surfaces or roll up in a ball to protect its soft under parts. Chitons are small mollusks that are common in all rocky shores of the tropics. They are nocturnal and move around the rocks at night feeding on algae. Their strange appearance is reminiscent of the ancient Fig. 69 granulata. trilobytes of prehistoric times. They are commonly introduced into the home with live rock.

Class Gastropods73 (Gk. gaster, belly; pous, foot): the intertidal zone is the high energy zone, thus, organisms living here are adapted to withstand intense ultra violet radiation, desiccation and high salinities. There is usually water retained in tidal pools even at low tide. Gastropods are very common in this zone, and usually the most conspicuous inhabitants. The sandy bottoms of the lagoons are often in deeper waters, covered with a mucous film rich in bacteria or of a carpet of Cyanobacteria where tufts of filamentous red algae such as Polysiphonia, Ceramium mingle. It is a hotspot for grazing and browsing fauna and their predators. Family are one of the more well known of herbivorous molluscs. The shells of this Family fall into six quite distinct Genera, each having a popular name; e.g., Strombus (“”), Lambis (“spider shells”), Terebellum (“torpedos”), Tibia (“shinbone shells”), and Varicospira (“beak shells”). Taxonomically they belong to the class Gastropoda, subclass Prosobranchia, order , superfamily Strombacea, family Strombidae Fig. 70a Family (predative murex) encompass a diverse and distinct group of Strombidae worldwide mollusks consists of five subfamiles, which are then further subdivided into more than 90 genera. Taxonomically they belong to the class Gastropoda, subclass Prosobranchia, order Caenogastropoda, superfamily Muricacea, family Muricidae. Family Cassidae (helmet shells, bonnets, helmschnecke) are a relatively small group of marine mollusks, but include some of the largest molluscan species. Fig. 70b Muricidae Cassida cornuta, the type species of the genus, is probably the largest. The family consists of two and eight genera according to the most current literature. The Cassidae inhabit tropical and temperate oceans from intertidal to subtidal depths. As tropical Cassidae secret acidic mucus, they have been observed to feed on sea urchins. Family Volutidae (walzenschnecke) are a large family of extremely diverse mollusks. The Volutidae also vary greatly in size. Some species rarely exceed a few Fig. 70c Cassidae cm in length and others are among the largest known species of marine mollusks. As fast crawlers, all of them are carnivorous, feeding on small marine animals.

Fig. 70d Volutidae

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Family Cypraeidae73 has about 200 living species. The basic shape of the shell is the same in all species. A very deep coating of enamel on the outer surface gives the shell a brilliantly polished appearance, naturally. In life, two lobes of the cowrie’s mantle extend out and over the dorsal surface of the shell, meeting at midline, and they continually deposit enamel while protecting the shell from abrasion. Interestingly, the mantle has a totally different color pattern than the shell. Fig. 70e Cyprea If startled or touched the cowry can suddenly change colors by withdrawing its tigris mantle completely inside the shell, thus confusing a predator. Family Turbinidae73 includes also star shells and are rather unique in being markedly flattened and in showing a lenticular edgewise appearance. Ever- widening whorls leave a deep umbilicus open to the tip of the spire, which can accommodate a beehive shaped that is chitinous (horny) rather than calcareous. The mollusc lives in shallow sands and is fairly widely distributed in Fig. 71a the warmer waters of the West and East coasts of North and South America, and in Monodonta the Indo-Pacific regions. Shells of the genus, Heliacus, more resemble those of the turbinata Trochidae family. The operculum is quite different in being a chitinous spiral of several turns. Turbo setosus is a commonly found species of the reef crest; with its robust shell it

is perfectly adapted to the rough conditions at the luvward side. Fig. 71b Turbo Taxonomically they belong to the class Gastropoda, subclass Prosobranchia, order setosus Archaeogastropoda, superfamily Trochacea, family Turbinidae. Family Cymatiidae (giant triton): Charonia tritonis has been historically used by humans as a signal horn and today is a rare but questionable collectors item. Its populations have been declining through massive exploitation. The triton is immune to the sea stars toxin (e.g. Acanthaster planci = Crown of Thorn) which to humans causes painful stings which last for hours and skin lesions not healing for months. During the day the triton rests hidden in the reef with a lid closing its shell. At night it roams the reef and finds the sea star by using its sense of smell. With it feelers and well developed eyes the triton evaluates the crown of thorns for an attack. The triton can move faster than the sea star in case it attempts to escape. The triton pushes its proboscis and front part of its shell under the sea star and turns it Fig. 72 Charonia over onto its back. Then the triton proceeds to devour the sea star entirely, spines tritonis feeding on and all. The relatively large weight of the giant triton locks the sea star in place and A.planci prevents it from fleeing. After 2 or 3 hours the triton has completely swallowed the poisonous mass of spines. Unfortunately, the tritons cannot effectively control mass outbreaks of the crown of thorns sea star even if they were in normal densities on untouched reefs. Feeding habits of A.planci (see also bioerosion, p.58/59): it preys exclusively on coral by everting stomach. It is normally uncommon on Pacific reefs crown-of-thorns is subject to massive population explosions in which hoards sweep across a reef. A.planci prefers branching, rapidly growing corals, but will take massive forms after depleting others. Affected reefs will be totally devastated by outbreaks, leaving bare framework open to bioerosion and physcial destruction; e.g., Guam, 1969: 90% of living corals killed off along 38 km of coastline down to 65 m. Recovery of devastated reefs is slow, 20-40 yr. Hypotheses for Acanthaster outbreaks range from human interference (removal of triton shell or puffer fish predators; excavation and dredging of reefs, opening sites for larval settlement) to natural, cyclic phenomenon. Control by success of larval recruitment, dependent on nutrient input from terrestrial runoff, which triggers plankton blooms.

Order Opisthobranch (Gk. ophisten, behind; branchia, gill): gastropods comprise a large and diverse group of marine snails and slugs, including some of the most beautiful and most specialized forms. The most recognizable to non-specialists are perhaps the sea slugs, or nudibranchs, and the pelagic sea , or pteropods. Morphologically intermediate between the more traditional snails and the shell- less nudibranchs are the “bubble-snails,” belonging to the Order Cephalaspidea. The adult stage in nudibranchs has completely lost both the shell and operculum. They share this character with the plant-eating sacoglossa or ascoglossa, which are not covered here. The loss of the shell has allowed a diverse array of body forms within this order. The Nudibranchia is divided into the following four suborders; the Dendronotacea, Doridacea, Arminacea and Aeolidacea. The name “nudibranch” means naked gills and the tail end of most sport a tuft of feathery objects that are the exposed gills that allow oxygen exchange. The front end is set off by a pair of feelers (rhinophores) and are exquisitely sensitive chemical receptors for prey, Fig. 73 Phyllidia dangers or potential mates. coelestis

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Class Bivalvia (L. bi, two; valva, valve) includs scallops, , mussels, and ; they comprise the second largest group of mollusks, yet are historically understudied relative to other mollusks. They are mega-diverse, comprising 8000-20,000 recent species in a wide variety of ecological and trophic niches. Bivalves are significant economically and ecologically: important aquaculture candidates, endangered and extinct species (freshwater mussels, Unionidae), and introduced pest species (zebra mussels). Despite their importance our understanding of bivalves as living invertebrate animals is fragmentary. Like other species of mollusks, many species are known from empty shells alone. More distant mollusc relatives are snails, sea slugs, , , cuttlefish and chambered . Family Tridacnidae (giant clams) are molluscs, they belong to the group that includes other bivalves, like the oysters, scallops, mussels, and other clams. There Fig. 74a Tridacna are seven species of giant clams found in the tropical Western Pacific and Indian sp. Oceans. The smallest species reaches only 15cm in length, while the largest species, Tridacna gigas, may grow to more than 1 m and weigh up to 300 kilograms. This extremely colorful species of is found in the Caribbean, and reaches a size of 8cm. They have an amusing method of propulsion which involves clapping their shells together to jet propel themselves through the water. They are like most of the bivalves filter feeders and feed on plankton and other nutrients in the water. Fig. 74b Lima scabra. Cass Cephalopoda (Gk. kephale, head; pous, foot); order Octopoda69 (Gk. octo, eight; pous, foot) devilfish (kraken) have rather short, compact bodies and only eight arms; no trace of the missing second arm pair remains even during embryonic development. All species are active at night, whereas many species are benthic (bottom-living) and crawl over the ocean floor with the mouth facing the substratum. Others alternate between a benthic and a pelagic (free-swimming) habitat and some species are completely pelagic. The two suborders of Octopoda are very different in Fig. 75a Octopoda appearance but there is little doubt that it is a natural group as the monophyly of the Octopoda is supported by a large variety of characters. The Cirrata is a group of deep-sea octopods commonly known as the “finned octopods” due to their large, wing-like . The Incirrata contain the common (benthic), shallow-water octopods as well as many deep-sea benthic and pelagic species. The most famous of these is the blue ring octopus (Hapalochlaena Iunulata, about 6 cm). The salvia of blue-ringed octopuses contains a powerful nerve toxic that blocks nerves from transmitting messages to the brain. The victim’s voluntary muscles Fig. 75b Hapalochlaena maculosa (involuntary muscles such as the heart, iris and gut lining continue to function) are paralyzed (people die from lack of oxygen). If mouth to mouth resuscitation is given, the victim recovers fully. Blue-ringed octopuses are shy and not aggressive, they tend to avoid people (they are not their natural prey – much too big!).

Order Nautiloids (Gk. nautes, sailer; eidos, form) family Natiloidea (nautilus): the chambered or pearly nautilus is a member of the class of the mollusks. The nautilus is a “living fossil” whose close relatives date back 100’s of millions of years into geologic history. The life and habits of the nautilus are, for the most part, a mystery, although a great deal has been learned about the nautilus in recent decades. For many years the nautilus was thought to be a rare deep water species, but recently they have been discovered in large numbers on Indo-Pacific reefs. They are nocturnal animals, swimming around the reef at night in search of small fish Fig. 76 Nautilus macromphalus and shrimp.

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Phylum Annelids71 (ringed worms): the worms are thought to have evolved from a primitive coelomate worm-like ancestor which developed metameric segmentation. The development of a coelom conferred many advantages, including acting as a hydrostatic means of locomotion. However, in the ancestral coelomate the force of muscle contractions in one area was carried throughout the body and so precise control of body movements was not possible. The phylum Annelida is divided into 3 classes: Polychaeta (bristleworms, mainly marine) Oligochaeta; (earthworms, mainly terrestrial) and freshwater Huridinea (leeches, mainly freshwater but with marine and terrestrial species of these); the polychaetes are thought to be closest to the ancestral form, (although, as we shall see, some of the polychaetes are highly specialized). The sea worms are a large and varied group of animals belonging to the . They are segmented worms, and all bear at least some resemblance to the common earthworm. In the ocean, however, the worms have evolved many different appearances. One of the more interesting varieties are the tube worms. These animals form a hard-shelled tube that provides them protection. The feather duster worms have a series of feathery tentacles on top that are used to filter nutrients from the water. When threatened by predators, they quickly withdraw deep into their tube homes. Another species, the Christmas tree worm, has a very ornate arrangement of feeding tentacles that can be found in a wide variety of bright colors. Some sea worms, such as the bristle worm, wander the sea floor with a covering of tiny bristles that can deliver a painful sting if threatened.

Family Terebellidae (fanworms, spagettiwurm): these meter-long polychaets are highly adapted deposit feeders and occur in soft bottom communities but are more widespread in temperate and coral reefs as crevice fauna, and associated with seagrass beds. They are all surface deposit feeders and may be highly selective. They have brightly colored feathery plumules. They are actually short and plump worms with sedentary habits. They have no proboscis as their food is collected by specialized feeding devices which evolved as part of the head. Only suitable sized particles are ingested while others are rejected through the mouth. They can extend their grooved buccal tentacles over substratum for a distance equal to the length of the body. Mucus secreted by the tentacles are used to prey upon living, planktonic organisms. They live in quiet places like the lagoons, rock pools or crevices where organic particles settle and are picked up by these sticky tentacles. Being tubicolous, the adult build fragile tubes out of sand, mud, shell fragments and sponge spicules with mucus heavily incorporated into them. The majority of the Fig. 77 Terebellidae tubicolous species are in contact with solid surfaces provided by shell hash, gravel, seagrasses, algae and sponges. Their tubes are found under large rocks or in cracks and crevices.

Family Spirorbidae (christmas tree worms, Spirobranchus giganteus) have an elaborate crown of spirals of feather-like tentacles/gills surrounds their tree-shaped body. When the worm is attacked or approached, the gills snap in and close a calcified trap door (operculum) to the tube to protect the actual worm from danger. At the base of their fans, the worms have a collar folded over the rim of the tube. As the worm grows, this collar adds layers upon layer of calcium salts embedded in slimy protein cells. The Spirorbidae tubes are small, white, and tightly coiled spirals. The size of the calcareous tubes range from less than one mm to several cm in diameter. Their gills range from 3-6cm Fig. 78 Spirobranchus giganteus length. The photo illustrates the “Christmas Tree Worm”, a passive residing in a Porites colony member of the reef community. These worms actively extend their feeding structures to filter particulate matter from passing water currents. If disturbed, they rapidly retreat into their “worm tubes” which are passively constructed alongside the living coral

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Family Sabellidae (tube worm, feather duster, grosser röhrenwurm): worms with smooth tapering cylindrical bodies living in tough non calcareous tubes. The prostomium and peristomium are fused and have developed into a tentacular crown (bi-pinnate radioles) that often obscures a pair of grooved palps. There is no operculum. The peristome is often developed into a collar surrounding the base of the radioles. Ciliated cells on the branchial crown filaments secrete mucus that collects captured particles such as detritus and bacteria. Mucus particles are formed and move down the branchial filaments to the mouth at the base of the crown. Along the way the particles are Fig. 79a Sabellastarte magnifica sorted for the correct size to be eaten. The body is clearly divided into thorax and abdomen. Chaetae are winged capillaries and uncini. Note that the tentacular crown is easily lost during collection and preservation. Its leathery tubes reach a length of 15cm, with a plume of feathery brown and white gills about 10cm long. The large-eyed Feather Duster worm can be found growing in leathery tubes approximately 10cm long. The feathery gills are usually orange-red to reddish-brown in color with white tips.

Fig. 79b Potamilla reniformis Family Amprinomidae (bristleworm, fireworm): the fireworms get their name from the extremely painful stings they can deliver from the feathery bristles along their sides. After the sting, the pain and itching can last for weeks. Fireworms can usually be found under rocks and coral heads on the reef and generally reach a size of 30cm in length. In life it is pink with conspicuous white setae which detach readily and cause severe irritation, forming a protective mechanism. Some people have had serious infections develop after being stung by such fireworms. Fig. 80a Eurythoe complanata

Fig. 80b Hermodice carunculata

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Phylum Arthropods72 (Gk. arthro, joined; poda, feet): the world of the crustaceans is a world of bizarre shapes and adaptations. arthropods dominate the oceans; so much so that, with the exception of only a few specialised species, no other arthropods are found in the marine environment. This group of animals is probably best-known for their hard outer shell. As the animal grows, this shell must be removed and discarded. Once this takes place, the new shell takes time to harden. During this period, the animal is without its primary means of protection and vulnerable to attack from predators. But they have an impressive arsenal of weapons at their disposal. The claw of many crustaceans is capable of exerting great pressures. Some even have the unique ability to produce a deafening miniature sonic boom with which they stun their prey. The mantis shrimp can even break the glass of an aquarium or split a man’s thumb to the bone with one strike. Order (Gk. deka, ten; pous, foot): a worldwide order of crustaceans (over 8500 species), with five pairs of thoracic appendages - anterior pincers and four pairs of walking legs. They include the shrimps and prawns (suborder: Natantia, “swimming forms”) and lobster, crayfish, and crabs (suborder: Reptantia, “walking forms”). Class . Family Majidae (arrow crab): these rather bizarre looking creatures get their name Fig. 81a from the triangular or arrowhead shape of their bodies. Their long legs gives them a Stenorhynchus spider-like appearance. They can reach a leg span of about 15cm, and are notorious seticornis for pulling feather duster worms out of their tubes with their long claws. Family Diogenidae (hermit crab, einsiedler krebse): the Hermit Crab is a curious species that carries its home around on its back. Because the crab’s abdomen is soft and vulnerable, its uses discarded shells to protect itself. As the crab grows larger, it must continually seek out larger shells. Hermit crabs are adept scavengers, and will feed on just about anything they find. Fig. 81b Dardanus Family Hippolytidae (cleaner shrimp, putzer garnele): the Cleaner Shrimp gets its megistos name from its behavior of cleaning parasites and damaged scales from many species of fish, including moray and large . Although it would make a tasty morsel, the shrimp is allowed to clean inside the fishes’ mouth in complete safety with no danger of being eaten. They are typically found in small caves in sheltered areas of the reef setting up cleaning stations for passing fish. These cleaning stations are manned by a large group of the shrimp. Fig. 81c Lysmata Family Grapsidae (purple shore crab) is commonly found on the open rocky amboinensis seashores of the pacific coast of North America. It has a purple and red shell with a white underbelly, and grows to about 5cm in length. This small crab can be seen scavenging the seashore where it feeds on algae and dead animal matter. Family Porcellanidae (porzellankrabbe, anemone crab): this small, colorful crab with a porcelain-like shell. Like the Clownfish, this crab has developed an immunity to anemone stings. This crab is usually found within the stinging Fig. 81d tentacles of a number of anemone species where it uses its large well-developed Hemigrapsus claws to keep clownfish from stealing its home. nudus

Order Isopoda (Gk. iso, equal; pous, foot): within specific habitats, the isopods frequently constitute a major component of the energy cycle, fulfilling roles of micrograzers, micropredators, parasites, and detritivores. In general, the suborders (Phreatoicidea, Asellota, Microcerberidea, Calabozoidea, Oniscidea, Valvifera, etc.) are herbivores or herbivorous scavengers, whereas the other suborders Fig. 81e (Flabellifera, Epicaridea, Gnathiidea, etc.) are carnivores, predators, and parasites. Neopetrolisthes Almost every animal of the coral reef ecosystem contains one or more parasite on ohshimai or in its body. They attach almost anywhere on their hosts, most notably to the skin, gills, and fins. Isopods tend to pierce into their hosts and feed on blood and tissue fluids, causing lesions. Fortunately, there exist species such as the cleaner , which swims over the entire body of the host fish, picking parasites from the scales. Isopod feeding habits are extremely diverse. In some areas of the world, isopods emerge from the benthos in large numbers at night to prey on (and frequently kill) diseased or injured fishes, as well as attacking fishes caught in commercial traps or nets (Stepien & Brusca 1985).

Fig. 82 parasitic isopod

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Phylum Echinodermata74 (Gk. echinos, spine; derma; skin): the echinoderms are a group of animals that includes starfish, urchins, feather stars, and sea cucumbers. They are simple animals, lacking a brain and complex sensing organs. Echinoderms are characterized by their radial symmetry and a central mouth. The coelom of the animals in this phylum is made from the digestive tube, not from cell masses. Therefore, echinoderms are . Although a looks round and has developed extremely sharp spines as a means of protection, closer inspection reveals that it is nothing more than a starfish with its legs wrapped inwards to form a sphere. Echinoderms have an endoskeleton, made of 95% calcium carbonate. Another hallmark of the echinoderms is hard, spiny skin. This is a common feature, but not always apparent in echinoderms. The uniting feature of echinoderms is a water-vascular system. This is a system of canals branching throughout the body that branch into many sections called tube feet. There are at least 2,000 tube feet, which can penetrate the body wall and skeleton in places called ambulacral grooves, in most echinoderms. These tube feet, and in many echinoderms arms and even organs, can be regenerated. The echinoderms are found in a stunning variety of shapes and colors, and are found decorating reefs around the world. Some of these animals are carnivorous, feeding on corals and scavenging the ocean floor. Certain species of starfish actually extend their stomachs into their unwary victims in order to digest them. The feather stars and sea cucumbers are mainly filter feeders, catching what ever they can find floating in the ocean currents. All of the echinoderms move around with the use of thousands of tiny tube feet, many of which have suction cups on the ends.

Class Crinoidea (Gk. krinon, lilly; eidos, form): the sea lillies, feather stars are the most primitive and oldest class. They consist of both deep sea lilies and tropical feather stars. These represent the earliest echinoderms, and are probably similar to a common ancestor of the entire phylum. The species that make up this phylum do not show body segmentation, and are radially symmetrical when fully grown but bilaterally symmetrical in the larvae stage. Almost all of the species are marine, although a few can live in brackish water.

Fig. 83a Crinoidea

Family Mariametridae (feather stars) is an unusual species that looks more like a plant than a starfish. It ranges in color from brown to orange, yellow, and black. Like the basket star, the feather starfish is a . It is nocturnal, and at night it can be found with its long arms unfurled where it filters plankton from the water.

Fig. 83b Lamprometra palmata Class Ophiuroidea (Gk. ophius, serpent; eidos, form) brittle stars (schlangensterne): these species have very flexible arms that are used for walking. These arms lack ambulacral grooves, differing the brittle stars from the sea stars. The species that make up this phylum do not show body segmentation, and are radially symmetrical when fully grown but bilaterally symmetrical in the larvae stage. Almost all of the species are marine, although a few can live in brackish water.

Fig. 84a Ophiuroidea

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Class Echinoideae (Gk. echinos, spiny; eidos, form): sea urchins have a number of predators on coral reefs as well, including molluscs and fish. It is difficult to imagine a predator being able to penetrate the terrifying arsenal of poisonous spines of Diadema urchins, but there are several fish which can make a meal on this unlikely prey, including porcupine fish (Diodon hystrix), and several triggerfish. Some of these fish are able to penetrate the spines, but most feed by turning the urchin over, and going into the shell through the soft tissue surrounding the mouth. For example, the Indo-Pacific titan Fig 85a Diadema setosum of the triggerfish (Balistoides virescens) is able to flip an urchin over by Indo-Pacific ejecting a strong jet of water while the urchin is relaxed. While some urchins are active during the day, and some during both day and night, most tropical urchins are nocturnal foragers. On Indo- Pacific coral reefs, it is not uncommon to find sea urchins such as Diadema taking shelter in crevices, or forming defensive aggregations during daytime, but coming out at night and dispersing over the reef to feed on algae and sea grass. Some of the slate pencil urchins seem to disappear entirely from the reef in the day, but appear again as if by magic at night. Sea urchins play an important Fig. 85b of role in the ecology of coral reefs. A variety of species inhabit the reef the Atlantic environment, each one occupying a slightly different habitat, or feeding on a slightly different type of food. Their presence, together with the presence of a group of herbivorous fishes, helps to keep the coral reef from becoming overgrown and smothered with algae. Without this group of herbivorous fishes and sea urchins, coral reefs as we know them, could not exist. However, when reefs become overfished as a result of poor or non-existent management practices, urchin populations may explode unchecked. At such artificially high densities, urchins may graze in habitats normally protected from grazing. They may also graze on live coral, Fig. 85c Heterocentrotus or damage and kill live coral in their movements in search of a mammillatus limited food supply. Populations of tropical Diadema urchins expanded on some reefs of the Egyptian Red Sea during the 1970’s, and destroyed large areas of coral, completely altering the reef environment. It is thought that the collection of porcupine fish for the curio trade may have depleted populations of this predator, and that this in turn allowed the urchin populations to explode. Nature is rarely that simple, but it does seem likely that the removal of a suite of predators from the reef may have played a role in the urchins’ unchecked increase. Similar increases in urchin abundance have also been recorded on Caribbean reefs, and on reefs in the Comores.

Class Holothuroidae (Gk. holothourion, sea polyp) sea cucumbers, (seegurken, seewalzen) are an abundant and diverse group of worm- like and usually soft-bodied echinoderms. They are found in nearly every marine environment, but are most diverse on tropical shallow- water coral reefs. They range from the intertidal, where they may be exposed briefly at low tide, to the floor of the deepest oceanic trenches. Considerable diversification has occurred since then with about 1400 living species in a variety of forms. Some of these are about 20cm in length, though adults of some diminutive species may Fig. 86 Synapta maculata not exceed a centimeter, while one large species can reach lengths of 5m (Synapta maculata). Several species can swim and there are even forms that live their entire lives as plankton, floating with the ocean currents. Economically, sea cucumbers are important in two main ways. First, some species produce toxins that are of interest to pharmaceutical firms. Some compounds isolated to date exhibit antimicrobial activity or act as anti-inflammatory agents and anticoagulants. Furthermore, the sticky Cuvierian tubules are placed over bleeding wounds as a bandage.Second, as a gourmet food item in the orient, they form the basis of a multimillion-dollar industry that processes the body wall for sale as Beche-de-Mer or Trepang. However, the high value of some species, the ease with which such shallow- water forms can be collected and their top-heavy age structures all contribute to over-exploitation and collapse of the fisheries in some regions. Fishermen in the Pacific islands use the toxins, some of which act as respiratory inhibitors, to entice fish and octopus from crevices so that they may be more easily speared.

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Class Asteroidea (Gk. aster, star; eidos, form): unlike the superficially similar brittles stars (Ophiuroidea), true starfish have no sharp demarcation between arms and central body, and they move using tube feet rather than wriggling movements of the whole arms. Most starfish are predators, feeding on sessile or slow-moving prey such as mollusks and barnacles. The aptly named crown-of-thorns starfish, Acanthaster (shown below), specializes on corals, and may do considerable damage to coral reefs. Many, but not all, starfish are able to turn a portion of their stomachs out through the mouth, and thus digest food outside of the body. Fig. 87a Fromia monolis Fromia monolis colorful orange and red starfish is one of the most common species. Its colorful markings and docile nature make it quite popular among aquarium hobbyists. This starfish grows to about 10cm in diameter, and is commonly found in the near where is feeds on small sponges and algae. The Cushion Star (Oreaster reticulatus) is a thick-bodied species of starfish with short legs. It ranges in color from brown to orange, red, and yellow. Its hard shell is covered with raised knobby spines. This starfish grows to a diameter of 25cm, and is found on the sandy bottoms. Fig. 87b Oreaster reticulatus The infamous crown-of-thorns starfish (Acanthaster planci) grows to over 30cm across and has 10-20 arms. It is well known for its voracious appetite for live hard-corals. At various times it has been blamed for the killing of large portions of reefs in parts of the pacific ocean, including a large portion of the Great Barrier Reef of Australia during the 1960’s. It is so despised that many scuba clubs organize “starfish hunts” in which these starfish are rounded up in an effort to save reefs from destruction. These starfish should be handled carefully, since the long, sharp spines are mildly venomous and can inflict painful, slowly healing wounds. One explanation for local population explosions of these destructive starfish could be the collection of this starfish’s natural enemy, the Fig. 87c A.placi shown here to Triton Trumpet (Charonia tritonis). For this reason trumpet feed on Porites sp. (if alive) should never be collected by divers and are often protected by law, because of their importance to reef ecology.

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Some other reef-fauna not mentioned so far: ecologically speaking, coral reefs are diverse places, containing 22 of the 23 animal phyla found on the planet. Symbiotic relationships are common and add to the complexity of species interactions. Coral reefs are among the most productive habitats, producing 2,000 decagrams of carbon per square meter per year, and the oldest, 400 million years.

Phylum Platyhelminthes (Gk. platys, flat; helminthes, worm): usually they are microscopic animals that live in numerous environments including the sea. Many species are parasitic and these are sometimes known as flukes. unsegmented worm-like animals with one opening to ingest food. The have flattened bodies and look more like chewing gum as they forage for food on the rocks. Class (L. turbellae, disturbance) mostly free-living and free-swimming for the whole of their life ciliated flatworms. They are found in a wide range of bright colors. These colors serve as a warning to potential predators because the worms excrete a foul- Fig. 88a Pseudoceros splendidus tasting mucus. The Red-rim Pseudoceros splendidus reaches a size of approximately 3-5cm in length. Gliding over the rocks and seaweed in the shallow sea, the Candy-striped Flatworm, Prostheceraeus vittatus, is occasionally seen by divers, and only very rarely reported by rockpoolers under rocks on the lower shore. The Candy-striped Flatworm is an active predator. It only grows to 50mm in length, but this is large for a planarian or flatworm, because most of them are parasitic on a variety of other animals including molluscs, crustaceans and fish in the sea.

Phylum Ectoprocta (moss animals) or Bryozoa66: refers to the mooslike appearance of many of he colonies. Some bryozoans encrust rocky surfaces, shells, or algae. Others, like the fossil bryozoans shown here, form lacy or fan-like colonies that in some regions may form an abundant component of limestones. Bryozoan colonies range from millimeters to meters in size, but the individuals that make up the colonies are rarely larger than a millimetre. Each body, or zooid, has a circular horseshoe-shaped lophophore and is largely covered with a chitonous cuticle that usually encloses a gelatinous, leathering, or calcified exoskeleton. Bryozoans are considered nuisances by some: over 125 species are known to grow on the bottoms of ships, causing drag and reducing the efficiency and maneuverability of the fouled Fig. 88b Ectorocta durig feeding ships. Bryozoans may also foul pilings, piers, and docks. Certain freshwater species occasionally form great jellylike colonies so huge they clog public or industrial water intakes. Yet bryozoans produce a remarkable variety of chemical compounds, some of which may find uses in medicine.

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Phylum Chordata75,76,77: are defined as organisms that possess a structure called a notochord, at least during some part of their development. The notochord is a rod that extends most of the length of the body when it is fully developed. Lying dorsal to the gut but ventral to the central nervous system, it stiffens the body and acts as support during locomotion. Other characteristics shared by chordates include the following (from Hickman and Roberts, 1994): • bilateral symmetry • segmented body, including segmented muscles; • three germ layers and a well-developed coelom; • single, dorsal, hollow nerve cord, usually with an enlarged anterior end (brain); • tail projecting beyond (posterior to) the anus at some stage of development; • pharyngeal pouches present at some stage of development; • ventral heart, with dorsal and ventral blood vessels and a closed blood system; • complete digestive system; • bony or cartilaginous endoskeleton usually present.

Subphylum Urochordata (Gk. oura, tail; chorde cord)75: the tunicates include a wide variety and, among other characteristics, are based on the presence of a larval notochord. The great majority are benthic sac-like filter feeders in the class . Most species filter water by a variety of mechanisms to extract fine planktonic food particles. Those within two much smaller classes (Thaliacea and Appendicularia), with some representatives listed here, are unique among the tunicates in that they have abandoned the benthic existence in favor of a holoplanktonic lifestyle. Class Larvacea (L. , ghost) or Appendicularia: includes a variety of Fig. 89a pelagic tunicates mostly inconspicuous, small pelagic tunicates. The body is formed by an oval-shaped trunk (often only about 1mm in length) and a longer tail, which is absent in thaliaceans. Class Thaliacea (German naturalist Thalius) order Salpida (salps) include the most commonly encountered pelagic tunicates. Salps can form massive aggregations of millions of individuals that may play a significant role in marine ecosystems. They exhibit among the fastest growth rates of any . A transparent test encloses the cylindrical body, and may be relatively thick and tough with projections and keels. Using rhythmic contractions of bands of circular muscles within the body wall, movement by jet propulsion is Fig. 89b picta accomplished by regulating the action of sphincter muscles that open and close anterior and posterior openings. This also serves to pump plankton-laden water through the body. Salps exhibit a complex life cycle with alternating aggregate and solitary generations. Aggregates (the sexual gonozooids) develop asexually from an elongating stolon that buds from an area just behind the endostyle of the solitary individuals (the oozooid). Individuals within aggregates are , typically starting as females that are fertilized by older male individuals from another chain. The resulting embryos (oozooids) then develop into the solitary asexual phase. There is no larval stage and even before release the young oozooid often has a developing stolon. In many species only a single embryo develops within each individual of the aggregate. This method of asexual reproduction enables salps to quickly exploit periods of abundant food with rapid increases in population density. With few defenses, rapid growth to maturity is the primary means to avoid by heteropods, jellyfish, siphonophores, ctenophores, sea turtles, marine birds and numerous types of fishes. Hyperiid amphipods and several species of fish also use salps as traveling homes. Other groups of thaliaceans include the doliolids (order Doliolida) and pyrosomes (order Pyrosomatida).

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Subphylum Vertebrata (L. verteratus, having a backbone) also known as Craniota; apart from their neural tube differentiated into a brain and spinal cord, have a vcranium (encapsuled brain); Class Chondrichthyes75 (Gk. chondros, cartilage; icthys, fish) such as , skates, rays, and chimaeras: their endoskeleton is entirely cartilaginous and all are carnivorous as exemplified by the great white shark (Carcharodon carcharias), the principle character in the "jaws" movie serials). There is perhaps no other animal on earth that evokes more fear in the mind of man than the shark. They are viewed as vicious man-eaters and are slaughtered the world over in an attempt to "make the seas safe". But of the hundreds of different species of sharks in the ocean, only a small handful pose any threat to man. Humans do not appear to be on the menu for sharks. It is thought that most shark attacks are a case of mistaken identity. A diver in a wet suit looks a lot like a sea lion, a favorite food for some of the larger sharks. The fact is that more people are killed by lightning each year then by sharks. Public fear and ignorance of these magnificent animals has led to many species being hunted and killed in large numbers. They have almost disappeared in some parts of the world. The Gray Reef Shark (Carcharhinus amblyrhynchos) is one of the major predators on the reef. Its highly streamlined body allows it a great deal of speed and maneuverability in the water. The Gray Reef shark is a very aggressive species, and is commonly seen in the classic "feeding frenzy" film footage. This shark can be identified by the black markings on its pectoral and tail fins. In startling contrast to the gray reef shark, the Whitetip Reef shark (Triaenodon obesus) is a timid and unaggressive species. This shark is commonly found near the floor of the reef, where it feed mainly on small fish, octopus, lobster and crabs. The Whitetip grows to a length of 150cm, and can Fig. 90a Carcharhinus be identified by the white markings on the tips of its fins. The Nurse amblyrhynchos Shark (Ginglymostoma cirratum) is a very docile and unaggressive species. It is a sluggish bottom feeder, and it uses its pavement-like teeth to crush shellfish. The Nurse Shark is commonly seen lying motionless on the ocean floor. It grows to an average length of 210cm, and is not considered dangerous to man. The Blue Spotted Stingray (Taeniura lymma) is a beautiful species, with brightly colored blue spots on its body. It is a relatively small ray, and can be kept successfully in an aquarium environment. There are few sites in the ocean as beautiful as the graceful flight of the (Manta hamiltoni) through the clear, blue waters. This magnificent animal can have a wingspan in excess of 450cm. Unlike Fig. 90b Triaenodon obesus its stingray cousins, the manta ray has no sting. They feed mainly on plankton and small schooling fish. The Ornate Wobbegong (Orectolobus ornatus) can be recognized by its body shape and coloration. It has a broad, flattened head with skin flaps around the snout margin. The eyes are small and oval (see bottom image). This species has two dorsal fins which are positioned posteriorly on the body. The caudal has a long upper lobe. The anal fin is positioned so far posteriorly, it almost looks like a lower caudal fin lobe. The intricate color pattern of the Ornate Wobbegong helps to break up the fish's outline. Even when illuminated by a flash as in the image, the mottled pattern on the tail helps camouflage the Fig. 90c Ginglymostoma fish against the sand and algae covered bottom. cirratum

Fig. 90d Orectolobus ornatus

Fig. 90d Taeniura lymma Fig. 90d Manta hamiltoni

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Class Osteichthyes76 (Gk. osteon, bone; icthys, fish): the bony fish are the most diverse and numerous of all . They differ from most of the cartilaginous fishes in having a terminal mouth and a flap (operculum) covering the gills. In addition, most have a swim bladder, which is ordinarily used to adjust their buoyancy, although among the air-breathing fishes it is attached to the pharynx and serves as a simple lung. The skin has many mucus glands and is usually adorned with dermal scales. Their jaws are well developed, articulated with the skull, and armed with teeth. Although the skeleton of most is bone, that of sturgeons and a few others is largely made of cartilage. They have a two-chambered heart built on the same plan as the Chondrichthyes (two-chambered with a Conus arteriosus and a sinus venosus). The sexes are separate, most are oviparous, and fertilization is usually external. There are two subclasses: subclass (ray-finned fishes) and subclass Sarcopterygii (lobe-finned fishes).

Family Labridae (Gk. labros, greedy or in L. lipp) , incl. cleaner fish): are common in the Atlantic, Indian, and Pacific. They have a protrusible mouth. Most jaw teeth with gaps between them; teeth usually jutting outward. Size, shape and color very diversified. Most species are sand burrowers; carnivores on benthic invertebrates; also planktivores, and some small species remove ectoparasites of larger fishes. Most species change color and sex with growth, from an initial phase (IP) of both males and females, the latter able to change sex into an often brilliantly colored terminal male phase (TP). Males dominate several females; all Indo-Pacific species are pelagic Fig. 91a Labroides dimidiatus spawners. Most species do well in aquaria, and young Coris are particularly popular. Maximum length about 2.3m (Chilinus undulatus = Napoleonfish), many are less than 15cm, the shortest being 4.5cm. Wrasses are carnivorous. Their diet consists primarily of parasitic copepods and other invertebrates that are taken from the mouth and Fig. 91b Aspidontus taeniatus gill openings of larger fish. They also feed occasionally on free- swimming crustaceans. Blue streak wrasses are known as common cleaner fish that set up cleaning stations on various parts of coral reefs, usually 0.5-3m. deep. They attract larger fish to their stations by making strange, oscillatory swimming movements, and the fish then stop to get cleaned. Wrasses enter the mouth and gill openings and remove any ectoparasites and diseased tissue. The larger fish not only refrain from devouring these small cleaner fish, but actually readily open their mouth and gill cavities so that they are able to clean. This is clearly a mutualistic relationship between cleaner wrasses and various larger fish of the ocean (Grant, 1978).Many cases of interspecific , in morphology as well as behaviour, are known from fishes. A famous example is the cleaner wrasse and its blenny mimic. While the cleaner Labroides dimidiatus (top) is a symbiont to other marine fish, removing their ectoparasites, the mimic Aspidontus taeniatus (below) bites off parts of other fishes' skin and fins.

Family Acanthuridae (surgeonfish): are brightly colored herbivorous fish (sometimes also called the tang). Circumtropical, especially around coral reefs; five species in the Atlantic, the remaining in the Pacific and Indian oceans. All have a deep compressed body with the eye high on the head and a long preorbital bone. Single unnotched with 4-9 spines and 19-31 rays; anal fin with 2 (only Naso) or 3 spines and 19-36 rays; pelvic fins with 1 spine and 3 (Naso and Paracanthurus) or 5 rays. Very small ctenoid scales. A small terminal mouth with a single row of close-set teeth. Most surgeon Fig. 92 Acanthurus nigrofuscus fishes graze on benthic algae and have a long intestine; some feed mainly on zooplankton or detritus. Surgeon fishes are able to slash other fishes with their sharp caudal spines by a rapid side sweep of the tail. They are pelagic spawners. Many species have bright colors and are popular aquarium fishes. In some surgeon fish, such as the unicorn fish, these razor like blades do not move, but appear as a bony curve that is quite poisonous. With the unicorn fish this curved blade appears like a horn of a unicorn pointing forward from the nose. When these surgeonfish are threatened by other species they will swim beside the intruder swinging their tails to inflict cuts. When their aim is accurate the intruder will receive long, deeply slicing cuts. When humans handle surgeonfish, extreme caution should be taken. Many unsuspecting persons has received deep wounds to their hands when attempting to remove this fish from a net or openly handle it.

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Family Pomacentridae (Gk. poma- opercle, centron, spine), refers to pointed margin of opercle and includes the damselfish (riffbarsch); chiefly marine; rare in brackish water. All tropical seas, mainly Indo- Pacific. One nostril on each side of head; double nostrils in some species of Chromis and Dascyllus. Body usually deep and compressed, with a small mouth and an incomplete and interrupted lateral line. Anal fin with usually 2 spines, very rarely 3. No palatine teeth. About 35cm maximum length. Coloration variable with individuals and with locality for the same species. Many species are Fig. 93a Pomacentrus coelestis highly territorial herbivores, , or planktivores. Damselfishes lay elliptical demersal eggs that are guarded by the males. Included are the anemonefishes (Amphiprioninae), which live in close association with large sea anemones. A massive presence of damselfish on the reef is a clear sign that the reef is under stress (Gk. amphi-, on both sides, prion saw, refers to serrate opercles); amongst the pomacentrids, are also found the clown- and anemonefish; the two-band Anemonefish (Amphiprion bicinctus) is bright orange to dark brown with two white or bluish-white bars, the first considerably expanded across the top of the head. Maximum recorded length is about 140mm. The anemonefish may have a similar pattern of other clown fish, but A. bicinctus differs from nearly all of them by having a yellowish caudal fin (it is whitish in other species). It also differs in the expansion of the first bar over the top of the head as opposed to the narrower bar of most other species. A. latifasciatus, from and the Comoro Islands is similar to the A. bicinctus in pattern and with its yellow tail, but the mid- body bar is much wider and the tail is forked. Amphiprion chagosensis from the and A. allardi from eastern Fig. 93b Amphiprion percula are also similar, however they have a white tail. A. bicinctus has been seen to be hosted by the following anemone species: Heteractis crispa, , Entacmaea quadricolor, Heteractis aurora, and Stichodactyla gigantea.

Family Balistidae (L. ballista, to catapult) the triggerfish are rather easily recognized by their flat, deep bodies, their small eyes placed high upon the head, and by their rough, rhomboid-shaped scales, often with small spines, which form a rough, tough covering on the body. Near the area in front of the tail they have some prickly, spike like, rows of spines. These spines can scratch and cause poisoning or other fish injury. They can also cause the fish to get snagged in a net, making it hard to remove them from it. Caution should be used whenever handling these fish. The Orange-lined Trigger (Balistapus undulatus) is actually the most aggressive of all the trigger species. Fig. 94 Balistapus undulatus Their strong jaws can reduce the hard shells of stony corals to piles of sand. Their striking colors can vary quite considerably. Indian ocean variants have orange tails while Pacific ocean versions can have orange-rayed fins. They grow to a length of about 40cm.

Family Chaetodontidae (Gk. chaet-, bristle; odont, tooth) the are some of the most beautiful colorful reef fish found along with their cousins, the Angelfish (Angelfish have a spur under each gill plate - see next page). Primarily Indo-west Pacific. Highly compressed body. Most with bright coloration, a dark band across the eye and an 'eyespot' dorsally. Generally near coral reefs, and typically diurnal. Many feed on a combination of coelenterate polyps or tentacles, small invertebrates, fish eggs, and filamentous algae while others are specialists or planktivores. Most species occur as heterosexual pairs. Pelagic spawners. Tholichthys larval stage with Fig. 95 ephipippium the head region covered with bony plates. The Saddleback Butterflyfish (Chaetodon ephipippium) is characterized by the large black marking on its back which somewhat resembles a saddle. The shape of this species resembles that of some angelfish species. The saddleback feeds on coral polyps and crustaceans.

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Family Pomacanthidae (Gk. poma, operculum; acanth, spine): are closely related to the butterflyfish, Angelfish can be easily distinguished from their cousins by the spur under the gill plates. Strongly compressed body. Angle of preopercle with a strong spine. Three spines in anal fin. Many species have an elongate extension on hind margin of soft dorsal and anal fins. Striking coloration, markedly different between juveniles and adults of many species. In shallow waters of less than 20m deep, very seldom below 50m; generally near coral reefs. All species studied to date are protogynous hermaphrodites with 'haremic' social system. Pelagic spawners. Fig. 96 Holacanthus tricolor Species of Centropyge feed primarily on filamentous algae and species of Genicanthus feed primarily on zooplankton; most others feed on sponges, invertebrates, algae and fish eggs. Most species do well in the aquarium, but some food specialists are difficult to maintain. The Rock Beauty Angelfish (Holacanthus tricolor) is characterized by its black and bright yellow colors. The juvenile of the species is yellow with a small dark spot. In the wild, this species grows to about 2 feet in length. Rock beauties are found in the western Atlantic, where they feed on algae, sponges and coral polyps.

Family (Gk. gobio, fresh water): ray-finned fish, gobies, chiefly marine and brackish, some species are catadromous (live in fresh water and enter salt water to spawn). Often the most abundant fish in freshwater on oceanic islands. Distribution: mostly tropical and subtropical areas. The smallest fishes (and vertebrates) in the world belong to this family. Mostly marine in shallow coastal waters and around coral reefs. Most are cryptic bottom dwelling carnivores of small benthic invertebrates; others are planktivores. Some species have symbiotic relationships with invertebrates (e.g. shrimps) and others are known to remove ecto-parasites from other fishes. Fig. 97 magnifica Typically nest spawners with non-spherical eggs guarded by the male. Many are popular aquarium fishes. The following subfamilies are recognized: Oxudercinae, Amblyopinae, Sicydiinae, Gobionellinae and . Firefishes (like this ) are characterized by their bright colors and by their unusually elongated dorsal fin. This fin is used as a signaling device to communicate with other firefishes. It is also used by the fish to wedge itself into small crevasses as a means of protection from predators. Firefishes are found throughout the Indo-Pacific.

Family Muraenidae (L. muraena, ): giant (riesen- muräne), it occurs on both lagoon and seaward reefs to depths of at least 46 m. It feeds primarily on fishes and occasionally on crustaceans. This is the largest moray eel, perhaps reaching 3 m in length. Because of its position at the top of the reef’s food chain it is often ciguatoxic (a skin toxin was noted in an Indo-Pacific moray eel). Itself it is the preferred food source of the octopods. Adults benthic, generally in shallow water among rocks and coral heads; Fig. 98 javanicus many species are more active at night and hide in holes and crevices during the day. Vicious reputation is undeserved, although some species will bite if provoked. Feed mainly on crustaceans, and small fishes. Larvae (leptocephali) epipelagic, widespread and abundant. Widely used as food, but a few large species may be ciguatoxic.

Familie Congridae (garden eel, röhrenaal), ein zu den knochenfischen (teleostei) zählende tiergruppe ist ebenso in diesen tiefen zu finden; in grossen gruppen bilden sie bestände die im weichem substrat sich bei gefahr blitzartig in ihre röhre zurückziehen. Fig. 99 Heterocephalus sp

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Fish in the Reef Ecosystem77: Impact of fishes in reef ecosystem is highly varied, with fish playing many roles on the reef stage. Moreover, the scene is constantly changing on the reef stage, so that the cast of characters is in constant change. We see this change most readily on a day to night basis, which is termed the diel cycle.

Reef by day: a scene crowded with diverse fish activity, with day active fish highly specialized in feeding behavior. A. Bottom feeders (benthic feeders): • Pomacentridae: damselfish, sergeant-majors; anemonefish • Gobiidae: cleaner gobies; • Chaetodontidae: butterflyfish; • prey on shelly benthos Labridae: hogfish, wrasses; Balistidae: triggerfish; Tetradontidae: pufferfish; • feed on sponges Pomacanthidae: angelfish; Zanclidae: ; • grazers Scaridae: parrotfish; Acanthuridae: surgeonfish; • sand bottom feeders Ostraciidae: trunkfish:, Botidae: flounder; Suatinidae: rays; • ambush predators: Batrachoididae: , toadfish; B. Waters above the reef (pelagic feeders): • Plankton feeders: Labridae: creole wrasse, Pomacentridae: chromis; Balistidae: durgon; Lutjanidae: snappers; • Stalking predators: Aulostomidae: trumpetfish; Belonidae: needlefish; Sphyraenidae: barracuda; • Other predators: Muraenidae: moray eels; Serranidae: groupers; Carangidae: jacks; Carcharinidae: sharks; • Some schooling fish like Haemulidae: grunts are inactive by day but feed elsewhere at night

Reef at twilight. A. About 1hr before sunset, night active fish take cover. 1. There follows a quiet period of ~20 min when midwater stage is relatively empty. 2. This is the time when predators have an advantage. B. About 30min after sunset, fishes like squirrelfish and bigeyes stream out of caves to feed in midwaters. Near reef, fish are protected from fast-moving predators, but move out at night.

Reef by night. A. Fish like bigeyes move offshore to feed. B. Other predators, like puffers, morays, feed closer to reef. C. Level of fish activity is much reduced. D. Many "actors" from daytime "soap-operas" rest by night, sometimes relatively exposed, or protected in a mucus-sheath sleeping bag (as do parrotfish, Scaridae).

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Class Reptilia (L. reptare, to crawl)78: the majority of marine reptiles are sea turtles; however, there are some sea snakes and some marine lizards (like those found on the Galapagos Islands). Sea turtles fall under the category of marine terapods which are marine organisms with four legs. Crocodiles and alligators also fall under this category. Most marine turtles are endangered or threatened and so it is important to take measures to keep their numbers from declining further. Many millions of years ago, long after the great reptiles had colonized the land, some of them decided to return to the sea. Today, reptiles are not the most common residents of the reef, but they are definitely among the most beautiful. Perhaps the most well known reptiles in the sea are the turtles. There are many different species of sea turtle, ranging in size from only 60cm to the real giants at over 150cm in length. Sea turtles lay their eggs on land. They can be seen on the beaches late at night digging a deep hole in the sand. The eggs are deposited and covered over. Several months later, the tiny turtles dig their way to the surface and scramble towards the sea. But a turtle's life is not easy, Only one in a thousand will survive the predators and return to the beach one day. Sea turtles were once killed by the thousands for food. Today, even though many face extinction they continue to be exploited. Their eggs and shells are in constant demand the world over. Another member of the sea reptile family enjoys full protection. The sea snake is the most venomous snake on earth. Several sea snake species can be found swimming the worlds reefs. Some of them are spectacularly colored. Divers are weary of this animal, but the sea snake is timid and will not attach unless provoked. Below is a list of some of the more common reptiles found on the reef.

Subclass Testudinata (L. testudo, tortoise) anapsid reptiles encased in a plastron and carapace; order Chelonia (Gk. chelone, turtle); Family Cheloniidae (Hawksbill Turtle) gets its name from its hawk- like beak. It ranges in size from 1m to 1.3m in length. This turtle's shell is the source of "tortoise shell", and because of this commercial exploitation has caused their numbers to dwindle. Their shell and oils are in constant demand, placing this turtle in danger. The hawksbill sea turtle as many other sea turtles is omnivorous, feeding both on plant and animal material. It prefers grasses and other plants from the bottom of the ocean as well as from grass beds that float at different Fig. 100 Eretmochelys imbricata depths. It also consumes small animals and sometimes the dead remains of marine creatures.

Subclass Diapsida (Gk. di, two; apsis, bar) reptiles with a diapsid or modified diapsid skull; order Squamata (l. squama, scale); Family Elapidae (sea snake) it can be found inhabiting most reefs of the world. Sea Snakes differ from terrestrial snakes in that their tails are flattened to form a paddle. This helps to propel them through the water. Even though the sea snake is the most poisonous snake in the world, they are not aggressive and rarely bite humans. This snake is a carnivore. It forages during the day, hunting by ambushing its prey. It is venomous snake, and it chews poison into fish and then swallows them. Fig. 101 Pelamis platurus

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Class Mammalia79 (L. mamme, breast) all mammals share three characteristics not found in other animals: 3 middle ear bones , hair; and the production of milk by modified sweat glands called mammary glands (mammals feed their newborn young with milk, a substance rich in fats and protein). Several million years ago, the first animals moved from the sea to colonize the land. Eventually, world-wide changes in climate and geography convinced some of the mammals to move back to the sea. These animals have since evolved to be perfectly adapted to their environment. Most of these animals comprise a group known as the cetaceans, which includes the dolphins and whales. The other main group of marine mammals fall into the pinnipedia family, which includes the seals and sea lions. Breathing air and then diving, cetaceans can hold their breath for unimaginable lengths of time. They are peaceful animals, and they are quite intelligent. These animals have exhibited remarkable abilities to communicate and learn. Their natural lives are spent in close family groups caring for their young and each other. Their songs can be heard echoing for miles beneath the waves. Below is a listing of some of the world's more familiar marine mammals. Order Celacea (L. cetus, whale) large massive mammals; pectoral limbs reduced to flippers, pelvic limbs lost, large tail bears horizontal flukes which are used in propusion. Family Balaenopteridae (humpback whale, buckelwal) the cerebellum of the humpback whale constitutes about 20% of the total weight of the brain; the brain does not differ much from those of other mysticete whales. The olfactory organs of humpback whales are greatly reduced and it is doubtful whether they have a sense of smell at all. Their eyes are small and adapted to withstand water pressure. Their external auditory passages are narrow, leading to a minute hole Fig. 102 Megaptera on the head not far behind the eye. Humpback females are larger than novaeangliae the males. They are one of the few species of mammals for which this is true. The most distinctive external features of humpbacks are the flipper size and form, fluke coloration and shape, and dorsal fin shape. Flippers are quite long and can be almost a third of the body length. They are largely white and have knobs on the leading edge. The -shaped tail flukes bear individually distinctive patterns of gray and white, and have a scalloped trailing edge. The dorsal fin can be a small triangle or sharply falcate, and it often has a stepped or humped shape; this is one source of the name "humpback." They are animals are quite large, growing to 18m in length. They feed on plankton, and are perhaps best known for their enchanting songs which can be heard for hundreds of km under the sea.

Family Delphinidae with 32 species placed in 17 genera, this is by far the largest family of cetaceans. Delphinids are small to medium- sized cetaceans, ranging from about 1.5m in length and 50kg weight to almost 10m in length and 7000kg. Males are usually larger than females. The shape of the head of many delphinids is distinctive; the forehead appears to bulge over the beak-like rostrum due to the presence of a lens-shaped fatty deposit called a "melon". This structure may help focus the sound emitted by these animals in echolocation and feeding. Other delphinids possess a melon, but their rostrum is short and the bulging forehead merely gives the head a Fig. 103 Tursiops melaena squared-off appearance. The bodies of most species are sleek and streamlined. Most have dorsal fins, which are usually curved (falcate), but much variation exists. The group includes bottlenose dolphins, killer whales, pilot whales, Pacific striped dolphins, and many more. The Bottlenosed Dolphin (Tursiops melaena) is perhaps the most familiar of the sea mammals. Their gentle nature has endeared them in our hearts.

Order Sirenia (Gk. a sea nymph that lured marines to their death) includes manatees and dugongs. Are marine herbivores with their long tail is horizontally flattened. Family Trichechidae (manatees) they are somewhat seal-shaped with forelimbs (flippers) adapted for a completely aquatic life and no hind limbs. Lungs extend the length of the animal's body, which is important in controlling position in the water column. Hair is distributed sparsely over the body and the surface layer of skin is continually sloughing off (believed to reduce the build-up of algae on their skin). The Manatee is a graceful and peaceful creature. They Fig. 104 Trichechus manatus feed on water plants, and inhabit the waterways and shores of Florida are found in the Indian ocean and the . They are slow creatures, and are in danger of extinction due to careless boaters.

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Part VI - Reef Responses to Environmental Parameters80 – Construction versus Destruction:

The first pages mostly dealt with the biodiversity of reef organisms and their construction over time. On page 5 of this document (constructive components of reef) some key elements are listed that contribute to the establishment of a reef structure; i.e. (1) foundation, (2) framework components, (3) encrusting Components, (4) bafflers and binders.

Coral reefs are constantly built and degraded by biotic elements (bioerosion). Bioerosion as such is not an entirely bad thing as it provides new substrate and raw material in order to allow rejuvenation of the reef structure. Synergistic effects that come from outside (greenhouse warming, pollution etc.) increase the overall stress balance which ultimately leads to the overall degradation of a reef (so called give up refs - see following section: “a balance between CONSTRUCTION vs. DESTRUCTION”).

Parameters favoring the “build-up” of reefs (constructon): In order to make sure that reefs proliferate at all; some major limiting factors on coral reef establishment have to be addressed first, growth and persistence of coral reefs are connected to:

A. Temperature • Restricted to waters warmer than 18oC, usually 26-28oC, and less than 36oC; corals are stenothermic organisms; at temperatures between 30-32°C, corals stop growth and reproductive activity to save energy (prolonged elevated temperatures cause bleaching = exocytosis of zooxanthellae, corals turn white). • Therefore, geographical limitation in-between 25o N and 25o S latitude. B. Salinity • Reefs require "normal" salinity ~35%o (parts/1000 = 35gNaCl per liter of water); heavy rainfall, river runoff can be lethal as salinity levels sink below this threshold level (mixohalinic zones). • Some reefs are adapted to higher salinity (40%o in euhalinic reefs) due to persistent evaporation and reduced water circulation. C. Light • Reefs require sunlight for vigorous growth (photosynthetic zooxanthellae alge). • Because light penetration decreases with water depth, reefs are restricted to shallow water, generally above 100m. • Some corals modify colony form in response to light, e.g. massive corals such as the Caribbean Montastrea annularis grow as rounded heads in shallow water, but forms flat plates in deeper water in order to improve light capture. D. Water motion • Reefs require constant water circulation and currents in order to obtain suspended food, oxygen, as well as the removal of sediments. • Some corals resist strong wave energy. • Some corals modify colony form in response to strength and pattern of water motion, e.g. Acropora palmata, the elkhorn coral of the West Indies, will grow as parallel-aligned branches, pointing in the direction of wave oscillation in areas where there is strong wave motion, but will form 3-dimensional colonies where wave action is reduced. E. Sedimentation • Heavy sedimentation can smother reefs. • High turbidity (suspended sediment) reduces light penetration. • Reef growth is reduced or absent along coastlines with high input of sediment from river runoff (e.g. Amazone river delta - BRA). • Corals have varying ability to shed sediment (see: D'Elia, Buddemeier, and Smith81).

Fig. 105 All dead surfaces of the reef are rapidly overgrown by a thin film of filamentous green algae. These form broad algal turfs that are a favorite diet of many fishes and urchins.

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Reef Degradation 82

Now we focus our attention to the degenerative forces acting upon a reef which ultimately may lead to the destruction of an entire reef section.

Destruction of reefs - ABIOTIC factors:

Chemical environment, the following chemical criteria modify the biocoenosis of a reef community: A. Carbonate mineral saturation: can affect coral calcification, skeletal chemistry/mineralogy; 1. dissolved CO2 in sea water will equilibrate the increased partial pressure of CO2 in the atmosphere, reducing carbonic supersaturation in tropical waters; increased CO2 results in larger H2CO3, ultimately slowing CaCO3 precipitation;

B. Salinity: corals are stenohaline (support only small fluctuations in salinity levels); 1. changes in rainfall, runoff alter salinities, often affecting reef growth; 2. elevated salinity from evaporation occurs on a local scale;

C. Nutrients: anthropogenic sources (chemical pollution in general) may trigger bacterially mediated diseases like (BBD) or cyanobacterial blooms (red tides); sources include fertilizer runoff, soil erosion, waste disposal have chronic local and regional effects; 1. phosphate affects coral skeletal growth; 2. nitrate promotes algal growth, tipping competitive balance away from corals; eutrophication causes the zooxanthellae to feed on N-sources of the eutrophicated water rather than on the N-metabolites of the coral host; this increases the competition between zooxanthellae and coral animals for H2CO3 and CO2, thus halting CaCO3 precipitation;

D. Oxygen levels: should be kept at optimum levels to avoid damages Fig. 105a Eutrophication on the to the sessile fauna; reef triggering algal blooms 4-8mL/L at the water surface due to photosynthetic activity and mixing with atmospheric layer; O2- consumption in flat lagoons deprived of zirkulation (at night and with low tide - as low as 1-2mL/L). E. Toxic/artifical compounds: anthropogenic sources; xenobiotica may act as growth inhibitors, mutagens, or sex modifiers; increased pollution has also contributed to mor commonly observable harmful algal blooms (HABs): Often, these events are accompanied by severe impacts to coastal resources, local economies, and public health (Raven, et al. 1992). In general, most harmful algal blooms are caused by plants (photosynthetic organisms) that form the "base" of the food chain. It is a challenge to define a harmful algal bloom and to characterize the species that causes it. Examples of HABs that are readily associated with water discoloration are blooms of many species of cyanobacteria, generally visible as floating green scums or colonies in coastal environments; two "brown tide" species (Aureococcus and Aureoumbra) that turn coastal lagoons dark chocolate brown; the dinoflagellates Alexandrium spp., Gymnodinium breve, and Noctiluca spp., that cause red water (red tides). However, no color is visible in other harmful species, such as the chlorophyll-free dinoflagellate Pfiesteria piscicida, several Dinophysis species, and benthic microalgae (e.g., Gambierdiscus) that grow on the surfaces of larger macroalgae in tropical waters (Burkholder and Glasgow 1997, Smayda 1997). In comparison, macroalgae are considered harmful due to dense overgrowth that can occur in localized areas, such as coral reefs of the tropics or coastal embayments Fig. 105b A "red tide" bloom of receiving excessive nutrient loading (LaPointe 1997, Valiella et Noctiluca colors the seawater. al. 1997). Accumulations can be so high as to cover the bottom Noctiluca is the largest of the of a region, excluding other biota as well as creating an dinoflagellates measuring about environment in which high oxygen consumption and the 2mm in diameter. associated anoxic conditions accompany decomposition of the accumulated or displaced biomass.

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Physical environment, the following physical criteria modify the biocoenosis of a reef community: naturally, such destruction is related to the interaction of energy possessed by waves, tides and currents with the frame- work of a reef system. Note that as one examines the distribution of energy across the reef (from deep forereef to shallow reef crest) the energy of wave systems progressively increases. Thus, the impact of waves across this section results in increased breakage and abrasion of the structures developed by corals and other reef organisms. A. Sea level rise: global eustatic rise predicted to be 8-29cm by 2030 and 50-150cm by 2100. Therefore rise in sea level is not of immediate concern as it has occurred in the past. Effects of sea level rise: 1. increased reef growth on reef flats, along coasts where current sealevels now act limiting; 2. deeper reefs unable to keep up; 3. changed patterns of coastal erosion, affecting intertidal ecosystems; 4. increased circulation and sedimentation in once restricted environments; 5. altered recruitment and composition of benthos; 6. modified shallow water habitats.

B. Temperature: a key variable, which is related to global (remember, corals are stenothermic organisms). Effects include: 1. unusual elevations can lead to bleaching, and subsequent death. Greenhouse effect may cause a rise of 2°C in the tropics for a doubling of CO2; even a fraction of this in sea surface temperature could be damaging to reefs. Other causes are El Nino (e.g. of late 1996/97 in Seychells and Maledives) or local anthropogenic effects; 2. synergism with light exposure documented and interactions with other parameters are likely; 3. lagoonal areas or other flat-water reef communities may experience increased temperatures during low tides when water circulation is shut off (atolls with a closed coral coverage).

C. Oceanic currents: wind-driven patterns determined by global climate regime; 1. control nutrient levels, temperatures, by upwelling, water mass advection. 2. transport reef propagules (vegetative reproductive fragments), affecting reef distribution. Storms and wave energy: increased wave action due to typhoons (= cyclones = hurricanes), quakes, and tsunamis: 1. provide a natural catastrophic pruning and/or substrate renewal; 2. influence succession and diversity; 3. wave energy reflects winds to affect reef growth.

D. Visible light required for photosynthesis in zooxanthella: light reduction can result from increased cloud cover, turbidity, or atmospheric pollution; 1. increased turbidity in the water column attenuates light to an extent that photosynthesis and calcification are reduced within a few meters to tens of meters; 2. reduced light penetration can significantly reduce optimum depth zones for reef growth. Ultraviolet light: destruction of stratospheric ozone layer is expected to increase surface UV exposure. 1. imposes physiological stress on shallow-water organisms; 2. may be mutagenic. 3. E. Mechanical damage: antrophogenic influences acting directly onto reef organisms; 1. achor damage, and damage caused by direct impaction (kollision with boats, tankers, freighters, etc.); 2. damages caused by the recreational industry (diving, snorkelling, etc. reef walking, sitting on coral heads), military or other commercial activity leads to chronic damages, irritations and ultimately results death of coral colonies. Fig. 106 Repair after a tanker crashed against a reef (top) F. Sedimentation: from rivers, building activity, fly-ash, coastal water run-off, etc.; 1. can reduce coral growth rates or totally smother corals; coverage of hard substrate by soft sediment can limit coral recruitment; 2. rise in sea level will cause increased erosion, sediment outfall onto reef areas; 3. many anthropogenic sources of sediment influx: dredging, deforestation (soil runoff), agriculture (eutrophication), Fig. 106b turbidity due to suspended construction (extra sedimentation). sediments

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Destruction of reefs - BIOTIC factors: inter- and intraspecific wars (see Kleemann VL …. /bioeros.pdf)82

The construction of the reef system is continuously counterbalanced by biodestructive processes. The reef is a community of organisms, all of which interact in a complex trophic (or feeding) structure. Some organisms can be major destructors of the reef simply as a result of their efforts to obtain food. For example, in addition to living tissues of the corals, algae and organic debris litter the reef surface which other animals actively use as foodstuff for their existence. Thus, a great variety of reef organisms act to destroy reef framework by biting, boring, excavating, rasping, etching, or scraping at the substratum. The process of destruction of hard reef substratum by organisms is called bioerosion. As bioerosion weakens the reef framework to a point at which it may collapse due to its own weight or as a result of storm activity (Goreau & Hartman, 1963), it occurs for mainly two reasons. 1. Protection: from intense predation pressure on reefs. As a result, much reef biomass and diversity is cryptic. Many borers of this type are permanently encased in their borings. 2. Feeding: biters, raspers, scrapers remove hard substratum in process of ingesting soft tissue of algae, coral. Borers and drillers penetrate shells to obtain goodies within.

Accordingly, biodestructive organisms can be broadly grouped into: Munchers and Crunchers: some animals, particularly the parrot fish and some starfish actively prey upon the living coral polyps. For example, it is common to hear the crunching of the strong parrot fish beaks as they clip the growing tips off of living coral branches. Similarly, the crown of thorns (A.planci starfish) everts its stomach around a branch of coral, secreting digestive fluids until the coral tissue is dissolved, and then absorbing this "coral broth" directly through its stomach tissues. In the normal reef setting, the growth rate of corals greatly exceeds the rate at which these organisms can destroy the reef. However, when the ecologic balances are upset and populations of these organisms increase beyond normal limits, their destructive actions can lead to the devastation of broad areas of the reef surface. Grazers: given the vast amount of algae that infest most surfaces of the reef, it is not surprising to have animals graze upon these fields of photosynthetic foodstuffs as part of their ecology. Perhaps most significant of these animals are the sea urchins, sea cucumbers, etc. (Echinodermata). In particular, the sea urchin possess a series of five teeth that serve as small scrapers and scourers that can actively break up the surface of the coral reef skeleton. It is common to find the stomach contents of these urchins to be filled with fragment of the coral skeleton. As a result, such feeding can be quite destructive to the reef. Borers: this is a unique life style whereby organism actively drill or etch into the dense skeletons of the coral reef. One example of such animals is the boring clam, Lithophaga which means "rock eater". If one were to cut a trench across the reef.....the dead and discarded skeletons of the reef corals are commonly riddled by numerous channels and tubes which were formed by these clams boring through the skeleton in search for food. Overall, this does not actively destroy the living reef structure and therefore is more of a passive process.

Methods of bioerosion. A. Chemical erosion is restricted to carbonates and mediated by proton activity (H+): 1. Drilling gastropods use chemical softening followed by rasping. 2. Clionid sponges dissolve out chips which are released to sediment (≈30% of lagoonal sediments). 3. Endolithic algae (BGA, GA, RA), fungi (occur deeper) B. Mechanical erosion is not restricted to CaCO3-substrata: 1. Scraping, rasping by means of radula (chitons, gastropods), jaws (echinoids). 2. Biting by parrotfish with strong jaws, predation on shells by crabs, birds, fish. 3. Boring by bivalves (Lithophaga, Gastrochaena, Tridacna), polychaetes, sipunculids, shrimp (Upogebia, Alpheus), barnacles (Lithotrya)

Fig. 107 bioerosive activity excerted by sea urchins on a Porites colony (left), endolithic activity due to microorganisms

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Competition: interaction for resources in short supply (food, space) between two species in which both are harmed or inhibited as a result of the interaction. A. Interphyletic (competition between phyla), interspecific (between different species) and or intraspecific competition (between same species): because of the intense competition for space on the reef, many corals have adopted methods by which to "stake a claim," and allow room for growth and expansion. These specialized tentacles are very adept at this purpose. Not only do the Euphyllia species form sweeper tentacles but Galaxea is known for its mere long thin threads. Aggression in corals (Lang, 1971, 1973). • Extra-coelenteric digestion of corals sitting next to each other. Fig. 107a Coral warfare against Done by extrusion of mesenterial filaments through polyp wall. intruders • A pecking order was established for Jamaican reef corals: 1. Solitary corals outcompete massive colonial species and fast growing branching species. 2. Aggressive ability allows slower growing species to maintain living space. B. Competitive networks (Jackson, Buss, Hughes): • Cryptic faunas of reefs: bryozoans, sponges, tunicates. • Long term studies of overgrowth and other competitive interactions between cryptic spp. done using artificial substrates. • Results showed not just linear hierarchies in competitive abilities Fig. 107b Sweeper tentacles in but return loops and networks in which some inferior competitors Euphyllia sp

may outcompete some spp. ranking above them. Effects of competition can be revealed when a grazer such as Diadema is removed (termed ecological release): Prior to 1983-84, Diadema antillarum was a major reef herbivore, grazing on algae, sometimes consuming live coral, in the Caribbean. Mass mortality, (disease ?) eliminated close to 100% of Diadema throughout Caribbean in 1983/84. Removal of this efficient grazer resulted in increased algal growth, boosting competition against corals. In absence of a controlling factor, competition can become a major force in shaping reef community.

Predation: predators of corals are more numerous than has been realized. A. Fish (development of septal spines in corals may deter predators): • Parrotfish (Scaridae) rasp live coral to 2-3 mm depth to feed on zooxanthellae, or bite off tips of branching corals exposing bare skeleton to bioerosion, so do triggers (Balistidae), filefish (Mona- Fig. 107c The colonial sea squirt canthidae), puffers (Tetraodontidae), and some wrasse (Labridae). Aplidium sp. is overgrowing a • Other fish predators include damselfish (Pomacentridae) which sea cucumber (prob. Eupentacta 2 cultivate algal gardens (1/4-1/2m per fish, entire colonies of sp.). damselfish can occupy a huge area on the reef), while the damsel feeds on coral polyps, leaving "kiss-marks" on coral, surgeonfish (Acanthuroidae), butterflyfish (Chaetodontidae). B. Molluscs: 1. Gastropods, Jenneria pustulata, Coralliophila abbreviata, C. violacea (has no radula, but suck polyps from skeleton), Cyphoma gibbosum (feeds on gorgonians), (let itself overgrow by the coral), Quoyula madreporarum (sessile snail that feed on coral tissue), Epitonium lura, E.replicata (have radula but suck polyps out of skeleton), Prinovula sp., Cyphoma gibbosum (gorgonian feeding snail), cornus (corallivorous). 2. Bivalves: Gastrochaena and Lithophaga etch their way into the Fig. 108 The sponge Stylissa coral, with only their siphons emerging at the top (“keyholes”); stipitata, being eating by the Tridacna crocea erodes reef substrate to form a grove where it nudibranch Discodoris heathi. can settle into, exposing just the fleshy mantle to the waters. 3. Nudibranchs: aeolids consume coral polyps and incorporate nematocysts and zooxanthellae. C. Fireworms: in Caribbean, Hermodice carunculata prefers branching Porites but will also take Acropora or Millepora. Damaged tips of Porites can be repaired by overgrowth, forming club-shaped branches.

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D. Crustaceans (mostly crabs): Mithrax sculptus in Caribbean; pagurids (hermits). E. Echinoderms: • Echinoids: sea urchins (E.lucunta, D.antillarum of the Caribbean, E.matei, D.setosum of the Indo-Pacific) can be a coral predator and source of bioerosion. • Asteroids: all Pacific (Acanthaster planci, Culcita coriacea, Choriaster granulatus, Pharia pyramidatus). F. Endolithic organisms: Fig. 109a The red sponge at the • Thallophyta are endolithic marine algae that etch their way into bottom is overgrowing and the carbonate skeleton; e.g. Ostreobium species gernerate the killing the grayish coral greenish band within the euphotic range shortly under the (Caribbean) coenosarc. • Porifera (Cliona sp.) are able to dissolve entire colonies within a short time and generate an enormous amount of fine carbonate sediments. G. Epilithic organisms: • Cyanobacterial species like Oscillatoria, Schizotrix, Microcolus, etc. actively try to settle on healthy coral tissue, triggering coral diseases due to a toxic shock (e.g. ). • Algae: the red alga Metapeyssonnelia corallepida, as well as the brown alga Lobophora variegata overgrow mainly Millepora Fig. 109b An ascidian (arrow) is complanata and M. alcicornis, but also other corals with smooth overgrowing a branching coral. surface, such as Porites porites and P.astreoides. In general, nutrient enrichment that causes eutrophication favors algal overgrowth of coral reefs. • Encrusting Porifera are known for their out-competing capability to overgrow coral colonies; Tepius sp ? even possesses endosymbiotic cyanobacteria (resulting in a toxic shock and is considered to trigger WBD in corals which ultimately can “mutate” to BBD); Chondrilla nucula is considered to be an epizoic spongy disease overgrowing coral heads. • Ascidiaceae: some ascidians grow upward by engulfing branching Fig. 109c Chondrilla nucula corals.

Anti-predation defenses among reef organisms. A. Diverse and well-developed. B. Toxins for self-defense: • 73% of species of sponges, tunicates, echinoderms from the western Pacific were found to be toxic to fishes. • Soft corals secrete toxins and show a hierarchy of toxicity. C. Morphologic defenses mechanisms: • Spinosity and shell strengthening in mollusks; more extensive in west Pacific than in Caribbean. • Spinosity, regeneration in comatulid crinoids. D. Nocturnal habits to escape daytime predators: • Comatulid crinoids, basketstars. • Nocturnal predators: octopus, morays, other fish. Chemical communication for the "peaceable" exchange of information as well as for chemical aggression and defense is by no means restricted to the terrestrial world: pheromones and allelochemicals are well known from fish, marine invertebrates, and algae. The coexistence of immobile organisms such as corals or sponges in complex communi-ties is to a large extent chemically mediated, their defense systems being made up of highly active allelochemicals. Some of these compounds exhibit exciting physiological properties which are of high medical and agrochemical Fig. 110 Clownfish and anemone interest. Mechanisms of adaptation, include tolerance and symbiosis, relationship feeding preferences, and chemical mimicry are all among the basic aspects of which are currently subjects of detailed study.

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Coral Diseases83: apart from the biotic and abiotic factors mentioned above (light, temperature, salinity, sedimentation/turbidity, substrate availability, nutrient levels, bioerosion, etc.) some other factors determine the successful establishment of reef communities: disease, and physical damage caused by anchor damage, SCUBA diving, dredging, etc. (Hallock et al. 1993, De Freese 1991, Jaap 1984, Glynn 1986, Lapointe 1997, Bell 1990). In order to understand the growing appearance of coral diseases and to stabilize at least the current status quo, coral pathology has to step out of its neglected existence to become a growing side-branch of coral reef science. Reefs are very sensitive to environmental conditions. They are adapted to extreme oligotrophic conditions. Under normal conditions, diseased or even dead corals never exceeds 5% of the total undisturbed reefs. But changes in coral health and vitality (disease, algal overgrowth, bleaching, etc.) may be more sensitive indicators of changing environmental conditions. All the man-made stresses (chemical and thermal pollution, sedimentation, dredging, blasting, boat anchoring, recreational activities, etc.) not only exert considerable pressure on these organisms, but also enforce the frequencies of coral pathogens. Thus, pathologic syndromes of reef corals are commonly grouped into those acting without and those mediated by a pathogen.

Disease working without a pathogen: although no pathogen is involved in the progress of the disease, the pathogenic reaction is caused by external influences as in the cases of Tissue Bleaching (TBL), Shut-Down- Reaction (SDR), and White Band Disease (WBD).

Tissue Bleaching (TBL): or tissue bleaching refers to the whitening of coral colonies brought about by a reduction in the number of zooxanthellae from the tissues of polyps, by a loss of photosynthetic pigment (exocytosis of zooxanthellae). Corals naturally loose less than 0.1% of their zooxanthellae during processes of regulation and replacement. However, adverse changes in a coral's environment can cause an increase in the number of zooxanthellae lost. This loss exposes the white calcium carbonate skeletons of the coral colony while the coenosarc is still present (a gentle touch reveals the presence of the living tissue - slippery feeling reveals the presence of coenosarc, a rough and sharp indicates a dead colony); depending upon the duration of the bleaching event, some zooxanthellae may stay in the dermal tissue of the coral host and may Fig. 112 Montipora annularis reproduce after the event is over. Under favorable conditions, corals (above) and Diplora may suvive even for an entire year without the algal symbiont. There labyrinthiformis (below). are a number of stresses or environmental changes that may cause Picture taken in Oct.1987 (left) bleaching including excess shade, increased levels of ultraviolet and after recovery in Aug.1990 radiation, sedimentation (necrosis in soft corals), pollution, salinity (right) - Key Largo FL changes, elevated atmospheric CO2 levels, industrial seawater pollution, excess freshwater runoffs, and increased surface water temperatures linked to the phenomenon known as ENSO (El-Nino – Southern Oscillation) events67, which causes TBL in the upper water layers (0-<15m) among coral (TBL in deeper water, without perceptible temperature changes, remain largely unexplained). Temperatures that stay around 33°C (sublethal level) block resettlement of zooxanthellae into the host; corals may survive for another few months. Temperatures above 34°C cause the immediate death of the coral colony, even though symbiotic algae may still reside within the dermal tissue of the organism. Sattellite telemetry allows to monitor sea- surface temperatures and makes it possible to track hot-spots and follow them as they migrate across the oceans (usually coupled with eddies that measure more than 100km in diameter).

Shut-Down-Reaction (SDR) - often referred to as Rapid Wasting (RW), Rapid- or Stress-Related Tissue Necrosis (RTN/SrTN), White Plague (WP), or White Death (WD). Observations in laboratory experiment and field observations ofcorals under sublethal (abiotic) stress such as elevated temperature, sedimentation, chemical pollution, have revealed that specimens can die from a simple scratch. Such sudden disintegration of the coral tissue, which starts at the margins of the injury, is characterized by sloughing off the tissue in thick strands of blobs from the coenosarc, leaving behind a completely denuded coral Fig. 122 Montastraea annularis skeleton. From the initial interface, the phenomenon proceeds in an looks like parrotfish bits? enlarging circle on massive corals, or moves along the branches in ramose forms, spreading to all side- branches upon reaching a junction. It is still unclear if SDR represents a disease on its own, as the thriggers match those in WBD or WS (see below), although there seem to be significant differences regarding the speed this disease affects a colony.

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Thus, SDR is especially dangerous as it can spread with an average speed of 10cm/hour – fast enough to be visually observed! Being contagious, SDR can be transmitted by a floating strand of dissolved, contaminated tissue to produce an onset on a neighboring stressed colony. Thus, triggering a catastrophic chain reaction, whichmay occur several times during the course of a season. It usually affects species of the Caribbean, such as small star corals stokesii, pillar corals Dendrogyra cylindrus, and boulder corals Montastrea annularis.

White Band Disease (WBD): as the name suggests, it refers to a band of white coral skeleton that represents a moving front of tissue destruction of scleractinian corals. Although less aggressive than SDR - it is not infectious and contagious, but advances with an average speed of a few mm/day. Several attempts at finding a distinct pathogen have been unsuccessful, although smears of WBD regularly yield a considerable variety of bacteria (GramPOS, GramNEG, and cyanophyta). WBD is strongly affected by abiotic conditions (e.g. temperature), and can be triggered by the settlement of blue-green Fig. 113 Acropora palmata algae which are toxic to corals. The site of settlement of blue-green algae is usually outlined at the interface of the coral corpus with the benthic sediment (shaded area, at the base of the coral). Settlement can also occur on damaged surfaces caused by external influences (wave action or damages caused by snorkelers or divers). An algal turf of green color, e.g. Chlorophyta, is considered harmless, whereas a dark pigmented algal overgrowth of Cyanophyta may trigger WDB. Reef structures affected by WBD can lead to a massive die-off, favoring tumors and is always accompanied by parasitic microorganisms (GramNEG rod-shaped bacteria, ciliates, protozoans, acoel turbellarians, , tiny copepods and amphipods) which result in algal overgrowth and subsequent death of the coral which are then successively colonized by invertebrates, gastropods, and boring clionid sponges (weaken the coral skeletons) and make them more susceptible to breakage during storms. Recent studies tend to further differentiate WBD into the classical form as type I and a somewhat altered form WBD-II; WBD-I: GramNEG rod-shaped bacteria were found in the tissues of affected corals. However, as mentioned above, the role of this microorganism in the development of disease has not been determined. WBD-II: in this disease, a margin of bleached tissue appears before the tissue is lost. Bacteria of the genus Vibrio have been found in the surface mucus of the bleached margin.

Diseases with pathogens: these involve the presence of a distinct disease causing agents; this group includes Bacterial Infections (BI) Fungal Infections (FI) and other epozoic organisms resulting in death of the coral colony.

Bacterial Infections (BI). Mucus production is the main defense mechanism against outside intruders and is important to fight diseases. But sometimes the mucal slime consisting mainly of glycopeptides, can lead to an unwanted cultivation of carbon and nitrogen feeding microorganisms, dominated by Desulvovibrio and species in its final stages. In sever cases, when attacked by Phormidium corallyticum it is almost certainly will infect the coral tissue with Black Band Disease (BBD - see below). Heavy microbial activity Fig. 114. it begins with the along with trapped sediments, quickly lowers the dissolved oxygen protective mucus layer as shown level of the closely surrounding waters, suffocating the delicate coral on this Siderastrea sidera tissue underneath. Only strong wave action or currents can save the coral by mechanically ripping off the slimy coverage within days after formation.

Black Band Disease (BBD): BBD is probably the best-known pathogenically caused . Similarly as in WBD a black band of "grazing" bacterium called Phormidium corallyticum (= Oscillatoria submembranacea a photosynthesizing, gliding, filamentous cyanobacterium) appears in association with other bacteria; e.g. cyanobacterium Spirulina sp. and proceed progressively outward, thus affecting the entire colony. Being contagious, BBD can spread easily to other corals by means of wave action. P.corallyticum eats its way from the upper surface where it spreads relatively fast, to Fig. 114a Diplora sp the edges of the coral surface. Under certain circumstances microscopic densely interwoven algal filaments (trichomes without significant cell wall constructions) of the pathogen form a blackish mat (predominantly on scleractinians of the family Faviidae).

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If enough light is available, to form a tiny algal spot, it gradually turns into a dark ring of tissue-stripped coral skeleton that proceed onwards with a few cm/week, enlarging the denuded area. Small corals can be deprived entirely of their living tissue, while larger ones can resist; once the black ring reaches the less illuminated flanks of the colony, due to lack of light, the pregression of the disease comes to a halt. In many cases the coral can fight BBD by producing an excess of mucus, thus starving the cyanobacterium. Sometimes the mucal slime (consisting mainly of glycopeptides, thus mainly substrate), can lead to an unwanted cultivation of carbon and nitrogen feeding microorganisms, dominated by Desulvovibrio and Beggiatoa species in its final stages. Heavy microbial activity quickly lowers the dissolved oxygen level of the closely surrounding waters, suffocating the delicate coral tissue underneath. Only strong wave action or currents can save the coral by mechanically ripping off the slimy coverage within days after formation. Although it is suggested that BBD may have a role in maintaining coral diversity because it is most prevalent in coral species that form large colonies and provide a structural framework for epibenthic organisms, BBD in combination with other diseases on a stressed reef can have devastating effects.BBD has a higher rate of infection in warmer water. Thus, not only seasonal temperatures, but anthropogenic disturbances as well (under eutrophic conditions even coral species immune to it are attacked) affect the spread of BBD. Similarly, as in WDB, consequently coral stocks suffering from BBD are also susceptible to tumors and parasitic worm infection.

Red Band Disease (RBD): as the name indicates, the "band" is a soft that is brick red or dark brown, not black, in color and easily dislodged from the surface of the coral tissue. This disease affects hard star, staghorn, and brain corals of the Caribbean and the Great Barrier Reef. The band in RBD appears to be composed of different cyanobacteria and microorganisms than those found in BBD with even the microbial mat movement being different; the types of microbes present might be altered depending on the coral host, but little is known about this. Several scientists are studying the Fig. 114b natans composition of these microbial mats to determine how they differ (looks like Platygyra sp) from BBD mats.

Black Overgrowing Cyanophyta (BOC): a number of other cyanophytic species like crustacea, C.scopulorum, Hormothamnium solutum, Langbia confervoides, L.semiplena, Phormidium spongeliae, and Spirulina subtilissima sometimes simply overgrow the coral, thus, starving the polyps. But in other cases they even actively penetrate and erode the coral skeleton, leading to the structural collapse of branching corals. In some cases, under eutrophic conditions, BOC is not only more common but may Fig. 114c Acropora sp. covered even trigger WBD. with a carpet of overgrowing cyanophyceae Black Aggressive Band (BAB): although similar in appearance to , antonius fragen BBD, the band material is somewhat thinner and appears gray rather Fig. 114d than black allowing the tissue-deprived coral to shine through. Recent studies revealed another cyanobacterial genus (Spirulina) as one possible cause, but it is not excluded that even a spirochete Ballesteros sp. could be the main pathogenic agent. High phosphorous contents in affected tissues suggest that eutrophication may be one way to trigger of BAB, since its appearance is closely related to shallow and coastal areas.

Lethal Orange Disease (LOD): a yet unknown bacterial pathogen causes death of the reef-building coralline algae Porolithon onkodes. This coralline alga is the principle cementing agent that maintains the intertidal wave-resistant reef crest. It helps the coral reef community by cementing together sand, coral fragments, and other debris into a suitable hard substrate for the establishment of coral colonies. It absorbs wave energy in the outer reef rim that would otherwise erode the shoreline and destroy many shallow-water reef communities. LOD leaves the coralline algae skeleton white as it progresses in an orange band, destroying the algae. When spreading, the front reaches the margin of the algal thallus, it forms upright filaments and Fig. 114e Coralline lethal orange globules, similar to those formed by terrestrial slime molds. disease

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The globules can be caught by waves and easily spread to nearby coralline algae Coralline Lethal Disease (CLD): it lacks the characteristic orange color of LOD, but is lethal, nonetheless. CLD is apparent as concentric white circles surrounding patches of green filamentous algae that have colonized the dead portion of the coralline algae Halimeda.

Fungal Infection (FI): fungal infestations on corals have been observed to occur along with other pathogens. A lower phycomycetous has been associated with BBD in certain star corals (Montastrea annularis); whereas BBD has been found to appear along with an ascomycetous fungus. Other cases which involve a hyphomycetous fungi (Scolecobasidium sp., Aspergillus sp.) are considered true fungal infections that affect only massive or platy corals. It forms necrotic patches (thus, termed also FIN) and reveal a zoned pattern. The top layer of the necrotic patch is overgrown with epilithic algae, sometimes intermingled with fungus. This is followed by a thin zone of fungal growth giving way to a green band of shell-boring algae. Beneath this strip lies a dense layer of fungal growth. The fungal zones above and below the green band (only about 0.5 to 1.5cm in width), appear brown to black and sometimes penetrate deeply into the coral skeleton. Fig. 115 Aspergillus colony on Gorgonia ventalina Yellow Band Disease (YBD also Yellow-Blotch Disease): it manifests itself as a broad yellow band moving across healthy coral tissue in a manner similar to the BBD. A band of decaying and sloughing off tissue is observed. However, the entire area denuded by the infection can retain the characteristic yellow color which can penetrate some millimeters into the skeleton. The YBD appears to be in no way similar to the aggressive LOD, which attacks coralline algae. Investigations into establishing a pathogen are underway. Species found to be affected by YBD are sclerectinians such as staghorn (Acropora sp., Porites sp.), honeycomb corals of the family Faviidae, plate corals (Turbinaria sp.), and even encrusting species of the genus Montastrea. Fig. 116 Porites sp.

Dark Spot Disease (DSD): it is based on increases in the occurrence of lesions and observations of loss of tissue associated with the spots. Dark purple to gray or brown patches of discolored tissue, often circular in shape but also occurring in irregular shapes and patterns, are scattered on the surface of the colony (bright purple patches have also been seen on bleached colonies) or appear adjacent to the sediment/algal margin of a colony. Sediment can accumulate in the centers of these patches, with bare skeleton occasionally seen when the sediment is brushed off. Investigations to isolate a distinct Fig. 117 dark spots on pathogen have not yet been successful. It could well be that a Siderastrea siderea combination of pathogens may trigger this disease.

Skeleton Eroding Band (SEB): a novel type of coral disease has been identified on Indo-Pacific reefs. It is caused by Halofolliculina corallasia, a new species of colonial, heterotrich ciliate that damages the skeleton of the coral throughout the Indo-Pacific and the Red Sea.. The syndrome is found on a wide variety of massive and branching corals, and progresses similarly as in cases of BBD but it is less dark and appears grayish rather than black. It feeds on bacteria that nourish themselves from the coral tissue of the colony. The skeleton eroding band consists of masses of black loricae (black Fig. 118 Acropora sp. shaped housings) of the ciliate, with bifurcated, beige wings sticking out, resembling a bed of microscopic garden eels (about 200µm). The dotted appearance of the white zone behind the front distinguishes SEB from BBD. SEB was found on reefs of the Sinai (Red Sea), Mauritius, (Indian Ocean) and Lizard Island (Pacific, GBR).

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Epizoism (EZ): Under certain circumstances, various epizoic organism were observed to overgrow living sclerectinian corals. The phaeophyta Lopophora variegata, the sponge Terpios hoshinota, the zoanthid Palythoa sp., some ascidians (e.g. Didemnidae), or the octocoral Erythropodium sp.. Although epizoism per se does not represent a disease, but is rather associated with interspecific competition, it is of perticular interest, as current antropogenically induced nutrient shifts and global warming may induce booming reproduction of faster Fig. 119a Epizoic sponge growing epizoic organisms by upsetting the existing a/biotic balance and ultimately altering a once flourishing coral reef from a "catch-up" reef to a "give-up" reefs.

Peyssonnelia (PEY): among recently described syndromes of epizoism on reef corals, one is caused by an unusual species of corallinaceal Rhodophyta, Corallinaceae. It is Metapeyssonnelia corallepida, a new species of a genus known only from the Mediterranean Sea. This epizoic disease destroys corals on reef crest areas, where it was not recorded at all 25yrs ago. M.corallepida is capable of overgrowing entire corals, a process half accomplished on the Millepora complanata. PEY forms a tightly attached "skin" on the coral surface without a trace of coral tissue left below the algal Fig. 119b Millepora complanata cover.

PNEophyllum (PNE): A coralline red algal species Pneophyllum conicum (Corallinacea) that like PEY overgrows and kills living corals. It predominantly occurs from intertidal reef-crests to depths >30m; and from sun-drenched upper reef surfaces deep into poorly illuminated caves. The color of the alga tends to correspond to the exposure to light (dark purple in the dark to gray at bright sites). It usually starts from the dead basal portion of the coral colony (or cracks and crevices) and expands its way up to the living portions. Usually this Fig. 120 Goniastrea retiformis corallinacea does not pose a threat to corals, but under certain overgrown by conditions (that still await demystification) can be quite lethal to most P. conicum Pocilloporidae, some Porites sp., and Faviidae ( Favia stelligera, , F.abdita, F.flexuosa, Goniastrea retiformis - fig.33, , P.lamellina, Leptoria phrygia).

Diseases involving a combination of various diseases

White Syndromes (WS): a disease characterized by the combining effects of WBD, TBL, and SDR. WS seems to be linked to the corallivorous snails Drupella cornus or Coralliophila violacea. It is suggested that WS-Drupella interaction occurs in three phases: Phase 1: D.cornus snail, when occurring in low numbers, are attracted by the disintegrating coral tissue and usually feed on the exact interface of WBD. Fig. 125 Drupella sp. Phase 2: larger concentrations of D.cornus feed on healthy tissue at a speed far exceeding that of WBD. Phase 3: the impact of excessive feeding by D.cornus triggers SDR, destroying more coral tissue than is occupied by snails; being stranded on a coral branch without tissue, the hords of D.cornus will move on to new feeding grounds.

Mutations and other Tissue Abnormalities: the white calcium carbonate skeleton of a hard coral is deposited by a thin layer of cells known as the calicoblastic epithelium. Skeletal morphology is primarily controlled by genetics. The shape of the skeleton which protects the colony of polyps varies with species, resulting in a number of characteristic shapes that allow even the non-professional observer to distinguish between many coral species. Skeletal deposition can change as a result of the actions of mussels, barnacles, christmas tree worms, and commensal crabs, all of which may bore holes in the coral skeleton and cause the coral to change the pattern of skeletal deposition. Other skeletal anomalies are caused by changes in the coral cells that deposit the carbonate skeleton. Two such changes are hyperplasia and neoplasia (cancer).

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Hyperplasia: a biological process that leads to an increase in the number of cells in a tissue or organ, thereby increasing the bulk of the tissue or the organ. A hyperplasm is a mass formed through the increase in the number of cells. It appears that such growth originate from a single budded polyp that undergoes localized, rapid growth, while retaining functional fusion of its tissues with those covering the normal colony skeleton.

Neoplasia: a pathologic process that results in the formation and Fig. 126 Diploria clivosa proliferation of an undifferentiated mass of cells. These cells grow and multiply more rapidly than normal and lack the structural organization and function of the normal tissue. These calcified protuberant masses on branching corals have lost their normal structure and have been shown to consist of undifferentiated calicoblastic epithelial cells. A study of the stable carbon isotope ratio of the calcium carbonate skeleton demonstrated that it was deposited in a very different manner, being laid down much more rapidly than normal; a finding consistent with the rapid metabolic rate of the tumor. White, protuberant, irregularly shaped, calcified masses or tumors, covered by a thin layer of translucent tissue, occur on the surfaces of branches of Acropora spp. and other members of the acroporid and pocilloporid families of hard corals. The cells found in the tumor resemble the more metabolically active Fig. 127 Acropora palmata and rapidly dividing cells of the growing branch tips, and like the branch tips, also lack the symbiotic algae. The epidermis covering the tumor also loses the mucus secretory cells that help remove sediments from the coral surface. The result is that sediment accumulations lead to tissue death and invasion of the skeleton by algae and boring organisms. The presence of the tumors on a branch is also associated with a decrease in/or halting of branch tip growth, suggesting changes in the transport of nutrients in the colony. This locally invasive abnormal mass of tissue and unusually porous skeleton grows faster than the surrounding normal tissue and skeleton. It proceeds to destroy the polyps and cause the death of the coral tissue. Based on these factors, this condition has been termed a neoplasm (cancer), calicoblastic epithelioma.

Future outlook84: the ever-increasing world population and its dependence on natural resources are placing new stresses on reefs at an accelerating rate. While these systems are surprisingly resilient, increasing levels of human impact in the form of elevated nutrients and sedimentation are taking their toll. Recent episodes of coral bleaching have brought national attention to the perils of tropical Fig. 128 Coral reefs in danger over the next 40 years reef systems. The outbreak of the Crown-of- Thorns starfish (A.planci) on the GBR or the sudden die-off of the long-spined sea urchin (D.antillarum) in the Caribbean have forced us to weigh the likelihood of these result from man-induced stresses versus natural ups and downs in the organisms that populate our seas. The possibility that sea level may soon rise at a rate exceeding the ability of present-day reefs to keep up is a further cause for great concern. The resulting impacts on coastal populations that depend on the reef for food and protection from oceanic waves could be devastating. Whether the goal is to better understand reefs and how they have evolved through time or to protect these valuable ecosystems from increased degradation, places the processes discussed in this paper into a realistic spatial and temporal framework which is of paramount importance.

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Part V - References on the web: Coral reefs general facts / introductions: http://www-personal.umich.edu/~jbudai/reefs/geo100-syllabus.html http://141.84.51.10/riffe/futura/futura1a.html http://www.com.univ-mrs.fr/IRD/atollpol/ukintro.html http://www.aquacare.de/info/veroeff/kuerif/riffe.htm http://www-personal.umich.edu/~jbudai/reefs/geo100-syllabus.html http://www.enchantedlearning.com/biomes/coralreef/coralreef.shtml http://geo.uni-paderborn.de/seminare/saudi_arabien/achtze/achtze.htm http://www.geology.iupui.edu/academics/CLASSES/g130/reefs/EO.htm Picture gallery: http://www-biol.paisley.ac.uk/biomedia/text/txt_pictures.htm http://www.imagequest3d.com/catalogue/catalogues2.htm http://www.holchanbelize.org/photos.html http://www.puertogalera.net/ScubaDiveSites/Diving.htm http://www.mantaray.com/cleaning_station/ocean_slide1.html http://www.photolib.noaa.gov/reef/ Reef history: http://darter.ocps.k12.fl.us/classroom/klenk/Coral.htm why to study reefs: http://www.uc.edu/geology/courses/coralreef/notes.htm Part I - Cnidaria: 1) http://www.indira.de/riff/riff.htm 2) http://www.sbg.ac.at/ipk/avstudio/pierofun/transcript/riffe-bv.pdf 3) http://www.einsamer-schuetze.com/natur/tierforschung/borstenworms/borstenworms.html 4) http://www.nhm.ac.uk/hosted_sites/quekett/Special-reef.html 5) http://cushforams.niu.edu/Forams.htm 6) http://www.geocities.com/cotylorhiza/x_steinkoralle2.jpg 7) http://egersund.asterisk.no/~emil/cnidaria/lophelia_pertusa.html 8) http://atlantic.er.usgs.gov/habitat/openfile/htm/50.htm 9) http://www.animalnetwork.com/fish2/aqfm/1997/jul/shell/default.asp 10) http://www.science.ubc.ca/~geol313/lecture/reefs/rgrowth/rgrowth.htm 11) http://www.sprl.umich.edu/GCL/paper_to_html/coral.html 12) http://www.zoologie-online.de/Systematik/Metazoa/Cnidaria/hauptteil_cnidaria.htm http://www.bio.swt.edu/Lavalli/guides/phylum_cnidaria.htm http://www-personal.umich.edu/~jbudai/reefs/coral1.html http://biosci238.bsd.uchicago.edu/Lab1.html 13) http://www.sbg.ac.at/ipk/avstudio/pierofun/coral/family.htm http://www.coralreefnetwork.com/stender/corals/rice/rice.htm http://www.bishopmuseum.org/bishop/PBS/Oman-coral-book/ http://www.bishopmuseum.org/bishop/PBS/Oman-coral-book/Index/CorBkIndex.htm 14) http://phylogeny.arizona.edu/tree/eukaryotes/animals/cnidaria/anthozoa/zoantharia.html 15) http://www.ucmp.berkeley.edu/cnidaria/ctenophora.html 16) http://www.paed-quest.de/oekoriff/content/qual_au.html http://fp.redshift.com/pelagia/nematocysts.htm http://www.gifte.de/quallen.htm http://www.aqua.org/animals/species/jellies/bayjelly.html http://www.bio.swt.edu/Lavalli/inverts/lecfold/cnidarians2.html http://faculty.vassar.edu/~mehaffey/academic/animalstructure/outlines/cnidaria.html http://www.shef.ac.uk/tldg/cnidnew/cndphylum.htm 17) http://tidepool.st.usm.edu/crswr/trichocyst.html 18) http://www.tennis.org/Special/lifecycle.html 19 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/trachylina.html 20 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/siphonophora.html 21 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/scyphozoa.html 22 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/cnidaria.html 23) http://faculty.washington.edu/cemills/Hydromedusae.html 24 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/hydroida.html 25) http://www.cyberphyla.com/hydrozoa/ 26) http://www.ucmp.berkeley.edu/cnidaria/hydrozoasy.html 27 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/hydrocorallina.html 28) http://www.wetwebmedia.com/millepor.htm 29) http://www.kheper.auz.com/gaia/biosphere/cnidaria/hydrozoa/Hydrozoa.htm

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30) http://animaldiversity.ummz.umich.edu/accounts/physalia/p._physalis$narrative.html 31) http://www.bio.swt.edu/Lavalli/inverts/lecfold/cnidarians1.html http://fp.redshift.com/pelagia/illustrations.htm 32) http://egersund.asterisk.no/~emil/cnidaria/index.html#schypozoa 33) http://www.uni-hohenheim.de/~bahagish/Stauromedusae.htm http://faculty.washington.edu/cemills/Stauromedusae.html http://fp.redshift.com/pelagia/stauromedusa.htm http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/stauromedusae.html 34) http://fp.redshift.com/pelagia/aurelia.htm http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/semaestomeae.html 35) http://www2.hawaii.edu/~ortogero/jellyfish.html http://www.bio.swt.edu/Lavalli/guides/cassio.htm http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/rhizostomeae.html 36) http://fp.redshift.com/pelagia/cubozoa.htm http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/cubomedusae.html 37) http://www.ucmp.berkeley.edu/cnidaria/Chironex.html 38) http://www.ucmp.berkeley.edu/cnidaria/octocorallia.html 39) http://www.smarterdesktops.com/MarineLife/what_are_they.htm 40 ) http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/gorgonaceae.html 41) http://www.seaslugforum.net/dendfeed.htm http://www.aquarium.net/0998/0998_5.shtml http://www.animalnetwork.com/fish2/aqfm/1997/nov/wb/default.asp 42) http://www.ucmp.berkeley.edu/cnidaria/pennatulacea.html http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/actinaria.html 43) http://www.ucmp.berkeley.edu/cnidaria/actinaria.html 44) http://www.ucmp.berkeley.edu/cnidaria/zoanthiniaria.html 45) http://www.kheper.auz.com/gaia/biosphere/cnidaria/corallimorpharia/Corallimorpharia.htm 46) http://www.uni-hohenheim.de/~bahagish/Ceriantharia.htm http://ag.arizona.edu/tree/eukaryotes/animals/cnidaria/anthozoa/zoantharia.html 47) http://porites.geology.uiowa.edu/database/corals/glossary/comorph.htm http://www.biol.vt.edu/Department/research/faculty/Opell/Biol4454/IZ%20Web%20copy/Cnidaria/scleractinia.html Part II – biology of cnidaria, structural elements and morphology 48) http://www.a-m.de/deutsch/lexikon/mineral/carbonate/aragonit.htm 49) http://www.enchantedlearning.com/subjects/invertebrates/coral/Coralprintout.shtml http://www.cnidaria.org/cri/vocab.html http://hypnea.botany.uwc.ac.za/marbot/coral_reefs/reef-building.htm (skeleton) 50) http://www.pacificwhale.org/printouts/fsreef.html http://library.thinkquest.org/25713/asex-a.html 51) http://www.petsforum.com/IMA/CR13.htm 52) http://www.bridge-rayn.org/aquatic%20curriculum/AqEnvCoursePres/index.htm http://www.uncwil.edu/people/szmanta/research_8.htm http://www.uncwil.edu/people/szmanta/research_10.htm http://library.thinkquest.org/25713/sex-a.html?tqskip=1 http://www.animalnetwork.com/fish2/aqfm/1998/jan/features/1/default.asp 53) http://ww2.mcgill.ca/Biology/undergra/c442b/lect19/1.htm 54) http://porites.geology.uiowa.edu/database/corals/glossary/clform.htm http://www.newcastle.edu.au/department/gl/corals/corals.htm http://www.nmfs.noaa.gov/prot_res/PR/taxonomicfeatures.html http://www.nmfs.noaa.gov/prot_res/PR/coralidmanualfront.html 55) http://porites.geology.uiowa.edu/database/corals/glossary/clshape.htm http://www.bishopmuseum.org/bishop/PBS/Oman-coral-book/Chap3/CorBkCh3htm.htm http://www.sbg.ac.at/ipk/avstudio/pierofun/coral/morfacro.htm 56) http://www.guam.net/pub/live_spawn/info.html http://www.curacao-diving.com/diving/spawning.htm http://www.gbrmpa.gov.au/corp_site/info_services/library/resources/reef_snapshots/coral_spawning.html http://www.gbundersea.com/gallery1/gallery1.htm http://www.fishid.com/learnctr/corspawn.htm http://www.aims.gov.au/movies/spawning-01.html 57) http://www.thekrib.com/Marine/tyree_rhythms92.html 58) http://www-personal.umich.edu/~jbudai/reefs/coral4.html 59) http://www.coexploration.org/bbsr/coral/html/body_life_cycle_story.html http://www.aims.gov.au/pages/reflib/bigbank/pages/bb-09e.html 60) http://www.datz.de/aktuell/titelgesch01_00.htm

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61) http://www.jochemnet.de/fiu/OCB3043_38.html http://www.ucmp.berkeley.edu/protista/dinoflagellata.html http://cima.uprm.edu/~morelock/coralrf.htm http://www2.uc.edu/geology/courses/coralreef/notes.htm http://www.wfu.edu/users/derlme03/symbiosis/symbiosishtml.htm http://mars.reefkeepers.net/Articles/AlguesSymbiotiques.html http://www.jcu.edu.au/fmhms/school/pms/bchemmbiol/Academic_Staff/DY_LAB/Symbiodinium.html http://mtlab.biol.tsukuba.ac.jp/WWW/taxonomy/Phytomastigophora/Dinophyta/Gymnodiniales.html* http://www.nsm.buffalo.edu/Bio/burr/montipora.htm 62) http://www.aquarium.net/0998/0998_4.shtml Types of coral reefs 63) http://school.discovery.com/homeworkhelp/worldbook/atozscience/c/133320.html http://www.petsforum.com/IMA/CR06.htm http://www.starfish.ch/Korallenriff/Riffarten.html Part III - Reef zonation 64) http://www.uark.edu/depts/geology/waterworld/dbmlreef2.htm http://ozreef.org/reference/zonation.html http://www.geo.lsa.umich.edu/~kacey/ugrad/coral8.html http://cima.uprm.edu/~morelock/concept.htm http://www.geology.iupui.edu/academics/CLASSES/g130/reefs/images/f1519th.gif http://cima.uprm.edu/~morelock/7_image/20zoncar.gif http://www.geology.iupui.edu/academics/CLASSES/g130/reefs/images/f1520th.gif Flora 65) http://www.com.univ-mrs.fr/IRD/atollpol/commatoll/ukalgato.htm http://www.com.univ-mrs.fr/IRD/atollpol/ecorecat/ukalgues.htm http://www.com.univ-mrs.fr/IRD/atollpol/ecorecat/ukalgesp.htm http://www.coexploration.org/bbsr/coral/html/body_plants_algae.html 66) http://orion1.paisley.ac.uk/courses/Tatner/biomedia/units/mino15.htm http://www.ucmp.berkeley.edu/bryozoa/bryozoa.html 67) http://www.sbg.ac.at/ipk/avstudio/pierofun/atmo/El-Nino.htm fauna - invertebrates http://www.nhm.ac.uk/zoology/taxinf/browse/family/family_browser.htm http://www.coralreefnetwork.com/marlife/inverts/inverts.htm http://phylogeny.arizona.edu/tree/eukaryotes/animals/animals.html http://www.reefimages.com/Invertebrates_and_Scenes.htm http://www.marineatlas.net/inverts/invertindex.shtml http://www.graysreef.nos.noaa.gov/grhb/ecology.html (brief intro into reef ecology) Food web on the reef 68) http://www.coralreefnetwork.com/educate/shows/foodwebs/slide1.htm http://www.reefs.org/library/talklog/e_borneman_051098.html http://www-ocean.tamu.edu/~pinckney/PDF_627_01/Lecture_10.pdf http://www.chez.com/easa/personal/pc/theorie/ff.html Porifera 70) http://animaldiversity.ummz.umich.edu/porifera.html http://www.ucmp.berkeley.edu/porifera/poriferamm.html http://salinella.bio.uottawa.ca/BIO2121/Lectures/BIO2121_lcts_Porif.htm http://www.guam.net/pub/sshs/depart/science/mancuso/apbiolecture/27_Animalia/Porifera/porifera.htm http://salinella.bio.uottawa.ca/BIO2121/Lectures/_PDFs/BIO2121_lct04_Porifera_00b.pdf (good graphics) http://darwin.bio.geneseo.edu/~bosch/Coverpage/Courses/InvPorifera/sld001.htm http://www.sidwell.edu/us/science/vlb5/Labs/Classification_Lab/Eukarya/Animalia/Porifera/ http://www-biol.paisley.ac.uk/courses/Tatner/biomedia/units/pori1.htm http://www.seasky.org/reeflife/sea2a.html (good images) Annelida 71) http://www.museum.vic.gov.au/poly/terintro.html http://www.nhm.ac.uk/zoology/taxinf/ http://www.nhm.ac.uk/zoology/taxinf/browse/family/terebellidae.htm http://www.arl.nus.edu.sg/mandar/yp/EPIC/Terebellidae.html http://www.reefimages.com/Worms/00000059.htm http://www.graysreef.nos.noaa.gov/grhb/ecology.html http://www-biol.paisley.ac.uk/courses/Tatner/biomedia/units/anne1.htm http://www-personal.umich.edu/~jbudai/reefs/coral3.html http://www.seasky.org/reeflife/sea2c.html http://ozreef.org/directory/index.html#ANNELIDA

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Arthropoda 72) http://www.seasky.org/reeflife/sea2e.html http://www.livingreefimages.com/Page63a.html http://ozreef.org/directory/index.html#CRUSTACEA Mollusca 73) http://www-biol.paisley.ac.uk/courses/Tatner/biomedia/units/moll1.htm http://www.worldwideconchology.com/MarineGastropods.htm http://nighthawk.tricity.wsu.edu/museum/Gastropods.html http://www.gastropods.com/shell_pages/Taxon_pages/Class_GASTROPODA.html http://www.wetwebmedia.com/gastropo.htm http://research.amnh.org/invertzoo/research.html http://divegallery.com/ http://webpages.shepherd.edu/PVILA/Oceanography/nudibranch.html http://www.seasky.org/reeflife/sea2f.html (good images) http://tolweb.org/tree/eukaryotes/animals/mollusca/cephalopoda/coleoidea/octopodiformes/octopoda/octopoda.html Echinodermata 74) http://www.coralreefnetwork.com/marlife/inverts/echinoderm.htm http://www.botany.uwc.ac.za/presents/focuson/Urchin/ http://www.nhm.ac.uk/palaeontology/echinoids/index.html http://www.sidwell.edu/us/science/vlb5/Labs/Classification_Lab/Eukarya/Animalia/Echinodermata/ http://phylogeny.arizona.edu/tree/eukaryotes/animals/echinodermata/echinodermata.html http://www.ucmp.berkeley.edu/echinodermata/crinoidea.html http://www.enature.com/search/show_search_byShape.asp?curGroupID=8&shapeID=1073 http://www2.uc.edu/geology/courses/coralreef/notes.htm http://www.seasky.org/reeflife/sea2d.html http://divegallery.com/crownofthorns.htm Chordata 75) http://fp.redshift.com/pelagia/tunicates.htm http://animaldiversity.ummz.umich.edu/search/simple/ Chondrichthyes 76) http://cas.bellarmine.edu/tietjen/images/cartilagenous_fish.htm http://www.seasky.org/reeflife/sea2i.html http://www.marineatlas.net/sw_fish/sharks.shtml http://www.amonline.net.au/fishes/fishfacts/fish/oornatus.htm Osteichthyes 77) http://www.reefimages.com/Fishes.htm http://www.angelfire.com/mi2/fishtank/index.html http://cas.bellarmine.edu/tietjen/images/bony_fish.htm http://nypa.uel.ac.uk/fish-bin/fishgen.pl?speccode=6380 http://www.wetwebmedia.com/acanthurTngs.htm http://www.btinternet.com/~martytaylor/scuba/fish16.htm http://www.fishbase.org/search.cfm http://www.amonline.net.au/fishes/search.cfm http://www.marineatlas.net/sw_fish/Fish_index.shtml http://www.coralreefnetwork.com/educate/shows/slide_shows.htm http://www.manband-archive.com/triggers/ http://www.amonline.net.au/fishes/fishfacts/specfam.htm Reptiles (testudines) 78) http://www.cyhaus.com/marine/reptiles.htm http://www.seasky.org/reeflife/sea2j.html http://animaldiversity.ummz.umich.edu/chordata/reptilia/testudines.html Mammalia 79) http://animaldiversity.ummz.umich.edu/chordata/mammalia.html http://animaldiversity.ummz.umich.edu/accounts/megaptera/m._novaeangliae$narrative.html http://www.seasky.org/reeflife/sea2k.html http://animaldiversity.ummz.umich.edu/chordata/mammalia/cetacea/delphinidae.html http://animaldiversity.ummz.umich.edu/accounts/trichechus/t._manatus_manatus$narrative.html

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Part IV - Environmental parameters 80) http://www2.uc.edu/geology/courses/coralreef/notes.htm http://www.co2science.org/issues/vol2/v2n15_co2science.htm http://www.saj.usace.army.mil/projects/appbmareco.htm#_Toc488404214 81) Workshop on Coral Bleaching, Coral Reef Ecosystems and Global Change: Report of Proceedings. Organized by C.F. D'Elia, R.W. Buddemeier, and S.V. Smith. Maryland Sea Grant College Publication. 1991). Reef framework, calcification, construction and destruction (bioerosion) 82) http://www-personal.umich.edu/~jbudai/reefs/coral5.html http://state-of-coast.noaa.gov/bulletins/html/hab_14/intro.html http://www.ots.ac.cr/rbt/revistas/suplemen/caribe2/antonius.htm http://www.aquarium.net/0697/0697_1.shtml http://life.bio.sunysb.edu/marinebio/coralreef.html http://www.nmnh.si.edu/paleo/macintyre/belize.htm http://www.chemecol.org/society/science.htm http://www.sbg.ac.at/ipk/avstudio/pierofun/transcript/bioeros.pdf

coral diseases: 83) http://www.sbg.ac.at/ipk/avstudio/pierofun/aqaba/disease1.htm http://ww2.mcgill.ca/Biology/undergra/c442b/lect21/1.htm http://www.broward.k12.fl.us/miramarhigh/guidance/mhssite/magnetmarine1/allymar.htm http://www.broward.k12.fl.us/douglashigh/jpearcem2/jpearce5/mmccarthy5/disease.html (table) http://www.nmfs.noaa.gov/prot_res/PR/coraldiseaseIDallcard.html http://www.ots.ac.cr/rbt/revistas/suplemen/caribe2/hayes.htm http://www.aspergillus.man.ac.uk/secure/news.htm http://www.reefrelief.org/Image_archive/Coral_nursery/Elkhorn/Page4/CN1.html http://www.es.cornell.edu/harvell/research.html http://www.athiel.com/ybd/ybd.htm

http://www.sbg.ac.at/ipk/avstudio/pierofun/atmo/elnino.htm http://www.solcomhouse.com/ElninoLanina.htm http://www.marinebiology.org/coralbleaching.htm http://state-of-coast.noaa.gov/bulletins/html/crf_08/national.html Future outlook and reef threats 84) http://cima.uprm.edu/~morelock/coralrf.htm http://www.solcomhouse.com/coralreef.htm http://www.epa.gov/owowwtr1/oceans/coral/biocrit/cont.html http://coralreef.gov/threats.html http://www.nodc.noaa.gov/col/projects/coral/coraldata/Coral_datasets.html http://www2.uwsuper.edu/ccrs/Projects/Anchor_Assessment/Anchor_Damage.htm http://www.yale.edu/roatan/soil.htm http://www.reef.edu.au/ant/coralreefpaper.htm http://www.uvi.edu/coral.reefer/threats.htm http://www.marine.uq.edu.au/ohg/HG%20papers/Hoegh-Guldberg%20et%20al.%201997%20GBR.pdf http://www.bishopmuseum.org/bishop/PBS/Oman-coral-book/Chap5/CorBkChap5.htm http://www.reefs.org/library/talklog/e_borneman_051098.html http://faculty.nl.edu/jste/Jamaica/reef%20presentation1.htm http://esa.sdsc.edu/factcoral.htm http://www.geology.iupui.edu/classes/g130/reefs/NG.htm (diving public)

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