Chapter V: (implemented Sept.2005; in colaboration with Dr.Karl Kleemann) 5.0 - Main Page

Bioerosion of higher taxa: The focus in the past chapters aimed at the complex interactions occurring within tropical reef ecosystems. In particular, various stress momenta as a result of anthropogenically induced modifications and their effects onto the coral animal have been addressed. This chapter stresses the effects of predominantly higher taxa that interact with the coral holobiont. As outlined already in previous chapters, the ecosystemic balance within the reef is finely tuned. Again, human action can be accounted for the disturbed inter- and intraspecific communication patterns among organisms, which easily result in an altered ecosystem stability that is far from that observed in undisdurbed ecosystems (a process that can be compared with the extremely sensitive and labile points of inflection of bifurcation systems often encountered in chaotic systems compare chapter IV, figure 4.3).
A collective term that summarizes this process was coined by Neumann in 1966 where he documented erosion by means of biological procedures.5.1a Bioerosion is easily influenced by abiotic as well as biotic stress factors. In the long term, it can make all the difference when entire reefs flip from a so-called "catch-up" reef into a "give-up" reef (compare chapter III, fig. 3.13).

Bioerosion an often neglected aspect: In his treatise, Charles Darwin assigned the most adapted organisms the best chances of survival.5.1b However, today it is commonly accepted that in at least three aspects Darwin was wrong. One of his erratic conclusion regarded the uncontrolled reproduction of all living species. Accordingly, a vehement war, a continuous fight among surviving species about resources and living space must take place in nature. Another of his erratic assumption is closely related to the previous one; in the fight for existence, particularly among species belonging to the same or in close relationship assigns the victorious group of organisms the dominating role within that ecosystem, whereas inferior groups of organisms are simply loosing out. Darwin termed this course of events "natural selection" (later paraphrased also with the "survival of the fittest) it can be regarded as Darwins most drastic erratic assumption.5.1c From a biosemiotic point of view it is possible to group communication processes within a given ecosystem into at least three distinct categories; this include inter-, intra-, and meta-specific interaction. A high level of interpretation processes is thereby integrated, which regard both abiotic sensing, meta- and interorganismic signalling as well as response behavior. Thereby, apparently dominating species are able to interpret the manifold ecosystemic sign inventory more efficiently than less successful species. They do so by simply employing "interactive tools" that are obviously more suitable for given environmental conditions. Hence, species less capable to deal less efficiently with the physico-chemical sign language will decrease in abundance or are driven into distinct niches where their interaction capabilities are again beneficial for their survival. Unconditioned natural observation seems to confirm this approach. Thereby, it turns out that cooperation and communication in nature is more important than struggle for survival or competition of resources. Striking evidence for this perspective can be found in social communities, symbioses, cooperations among species of different taxa, among plants and animals as well as other forms of cooperation. This essential difference with regards to the Darwinian approach is a driving force behind bioerosive properties of tropical reef ecosystems.
Thus intense inter- and transspecific interaction within a reef ecosystem is a driving force for the evolution of cryptic lifestyles. Many of the bioerosive species are without toxins, armature, spines, and thick shells. Yet, they utilize physico-chemical means to degrade calcareous substrates. The huge eroding pressure by numerous corallivorous, endo- and epilithic species from all taxa - ranging from microbial endoliths to grazing vertebrates does occur and is an essential part even in undisturbed tropical reef ecosystems. Bioerosion is thus a key element for a holistic understanding of reef ecosystems in that bioeroders erode and release calcium-carbonate back into the environment, which is then re-used by other accreting organisms. However, this fragile balance between reef accretion and reef erosion is easily upset by abiotically or biotically interference, thereby further enhancing bioerosive processes (positive feedback loop). It has been suggested that the numbers and combined mass of bioeroding organisms equal or exceed that of the surface biota 5.1d. On the other hand, bioerosion provides innumerable small organisms (protozoans, flatworms, copepods etc.) as well as larger ones like feather stars, molluscs, crabs etc. niches in nooks and crannies. Countless fish also use corals to seek shelter (e.g. schools of juveniles) and venture out from branching corals whenever danger has subsided. In a healthy, actively accreting reef, bioeroders contribute enormously to the diversity of habitats within the reef structure. Bioeroders are important in sculpturing coral reef growth and in producing the sediments (rubble, sand, silt, and clay). However, if reef growth slows in response to natural or anthropogenic environmental stress factors, the dynamic balance is disturbed, inter- and transspecific communication distorted, which over the long run, leads to excessive bioerosion and ultimately may trigger the decline of entire reefs.

Bioeroder diversity5.2a: The prokaryotic- and abiotically mediated erosive properties of the living coral/coralline tissue have been outlined in the previous chapter. This chapter focuses on the relationship between microbial epiliths and endoliths (as the primary producers of the bioerosive community), and their grazers (see fig.5.1a). Thus, interphyletic competition (competition of corals with organisms of other phyla or even kingdoms) makes up large part of this discourse, it should not be forgotten that the synergistic relationship of various bioerosive processes are largely controlled by ecosystemic parameters; i.e. a healthy coral-community is a lot more tolerant to disturbances such as predation. In fact a huge grazing pressure by numerous corallivorous species, microbial detrivorous consumption of a diseased colonies, or even abiotically induced coral decay easily upsets the fragile balance described in previous chapters and thereby destabilizes benthic coral communities, which in turn trigger secondary bioerosive processes.5.2b

Bioeroder diversity includes members of all taxa. However, since most bioeroding species are both small in size and secretive in living habits, it has been suggested that their numbers and combined mass equal or exceed that of the surface biota.5.3 Due to the intense competition and predation within a reef ecosystem, selection pressure and niche specialisation have led to the selection and evolution of cryptic lifestyles. Many of the secretive species are without toxins, armature, spines, and thick shells. On the other hand, most associated coral fauna can be considered casual associates; i.e. innumerable small organisms (protozoans, flatworms, copepods etc.), larger ones like feather stars, molluscs, crabs etc. hide in nooks and crannies and emerge only occasionally to feed on passbyers. Countless fish also use corals to seek shelter (e.g. schools of juveniles) and venture out from branching corals whenever danger has subsided. In a healthy, actively accreting reef, bioeroders contribute enormously to the diversity of habitats within the reef structure (see Connels Intermediate Disturbance Hypothesis - Chapter-II). Indeed, bioeroders are important in sculpturing coral reef growth and in producing the sediments (rubble, sand, silt, and clay). However, if reef growth slows in response to natural or anthropogenic environmental stress factors, the dynamic balance is disturbed, with of erosion exceeding rates of accretion; over the long run, such a reef may cease to exist and the reef may cease to exist.5.5

 

 


Fig.5.1a: Bioerosive divsrsity (120kB) 5.6

Since corals provide a microhabitat for numerous organisms, it does not surprise that among those using corals for shelter, living space, or temporary retrieval sites, there are also those that utilize corals as a food source. As a result and apart from the essential important aspect of photosymbiotic associations among reef builders, the ecological diversity on reefs is also shaped by the diversity of their destroyers. For convenience, and depending on their location, bioeroders can be classified as:5.7

  • epilithic sessile species live on exposed limestone surfaces and feed directly upon invertebrates (epizootic) or algae by etching, rasping, or scraping and results in incidental skeletal or substrate damage;
  • chasmoliths occupy cracks and holes - they nestle in depressions, sometimes even on living sessile organisms (thereby deforming growth of the host); and
  • endoliths, which are the most cryptic, i.e. sessile organisms hidden within skeletons; endoliths are taxonomically the most diverse and include etchers (e.g. bacteria, fungi, and endolithic algae) and non-predatory borers (e.g. clionid sponges, bivalves, spionid polychaetes, and sipunculans); endolithic activity can be either chemical, mechanical or a process that involves both mechanisms.
Since Epiliths and Chasmoliths break down calcareous substrata directly or indirectly and in a variety of ways. The bioerosive property of these groups is consequently found across all organismic taxa.5.8a
 
In comparison to their prime target zones, bioeroders can also be grouped based on their main erosive methods:5.8c

Browsers predominantly consume plant tissue above a given substrate, with either a denuding or non-denuding effect. The most important denuders are some annelids (fireworms), some molluscs (corallivorous snails), some asteroids (corallivorous sea stars), some echinoids, and some fish (acanthuroids, rabbitfish, here siganids, and damselfish, e.g. pomacentrids).

Grazers on the other hand crop very close to a substrate, thereby ingesting substantial portions of algae, associated small invertebrates and even underlying skeleton. Many grazers capable of removing and ingesting calcareous material such as coralline algal skeleton include excavators (capable of deep excavation that remove large amounts of substrate), and scrapers (have weaker jaw apparatuses, and smaller bite size with limited substrate removal). The most important excavators and scrapers reducing substrate to fine-coarse sand are gastropods (e.g. limpets), molluscs (typically chitons), some regular echinoids, acanthuroids, and especially scarids (parrotfish). Apart from these major predators, corals can be also important food items for diadematid sea urchins.

 


Fig.5.1b: Spatial and temporal variations of browsers / grazers (100kB) 5.8b

Since most endoliths are borers that erode limestone mechanically, chemically, or by a combination of both processes a further distinction can be made. The macroborers are generally more conspicuous, and include numerous invertebrates and vertebrate taxa across the animal kingdom. The majority of endolithic invertebrates are suspension feeders, gathering their food passively or actively from the water column, while others, which include mobile predators such as naticid and muricid gastropods, produce boreholes as a means of access to prey. The mechanical destabilization of these internal borers not only causes premature collapse of branching corals but they are significant contributors in reducing the reef framework to silt and fine sand.5.9

Borers: Microborers include bacteria, Cyanobacteria, fungi, and algae (endolithic rhizomes with <100m in diameter). Macroborers include boring sponges, various bivalves, polychaetes, echinoids, certain barnacles, sipunculans, bryozoans, phoronids, coralliphilid gastropods, and some shrimps.
Among boring bivalves, sponges, polychaetes and barnacles that are capable of excavating into live corals, the clionid sponges are among the most common and active endolithic organisms. While bivalves and sponges exert their endolithic activity primarily via chemical means (etching) their full bioerosive properties are amplified by mechanical means. Although polychaetes can exert an important role on a local level, lithophagid (mytilid) bivalves are the most common particularly in the lowest intertidal and shallow subtidal zones. The macroborers found among other taxa include polychaetes, acrothoracican and thoracican barnacles, sipunculans, bryozoans, phoronids, coralliphilid gastropods, and alphaeid and callianassid shrimp.

Etchers: Bioerosion of calcareous skeletons that solely is achieved by chemical means is encountered among minute organisms, requiring microscopical methods for study, and are referred to as microborers or endolithic microorganisms. To this group belong three kingdoms, namely bacteria (prokaryota), fungi, and eukaryotic micro-organisms such as protista (foraminifers) and assemblages of endolithic green and red algae.

Although scleractinian corals are the dominant occupiers of primary space in coral-reef communities (with the remainder occupied by other sessile organisms such as soft corals, gorgonians, anemones, sponges, algae, etc.), their relative abundances are often determined by environmental parameters and the concomitant grazing activities of mobile invertebrates and vertebrate predators.5.10 Ultimately, the combined effects of these bioeroders determine the fate of a reef complex in particular areas or zones and at different times (compare fig.5.28). With bioerosion being a natural ever-present vector occurring everywhere on the reef, it is obvious that this dynamic balance between reef-builders and reef eroders becomes especially distorted under altered environmental conditions; i.e. in eutrophicated areas resulting in a shift dominated by scleractinian species, toward on in which soft corals, boring bivalves and/or sponges become the dominant elements (compare fig.3.7 - Chapter III).5.11

This brief categorization is now followed by a section highlighting the most prevalent bioeroders within a given taxon; first to be named are those from the Bacteria-kingdom, to be followed by those of the Fungi and Plant Kingdoms, only to be finalized by the huge kingdom of Animals.
 
Kingdom PROKARYOTA
As outlined by the bioeroding potential of epizootic MPSL-feeding Bacteria (as discussed in Chapter-IV), in-depth knowledge of endolithic microorganisms (that etch their way into the carbonate substratum), their diversity and function is still very limited.

Eubacteria: Several species of cyanobacteria (e.g. Hyella, Plectonema, Mastigocoleus, and Entophysalis) are capable of eroding reef rock from the splash zone to depths of at least 75m (fig.5.2).5.12 Cyanobacteria have also been implicated in the erosion of lagoon-floor sediments on the GBR, amounting to the dissolution of between 18% and 30% of the sediment influx rate. The main bioerosive capacity is achieved as they etch the surface of limestone crystals and dissolves the organic matrix to enter the coral skeleton (fig.5.2). Brownish skeletal areas (associated with endolithic sponges) inside massive corals contained from 10-100E3 bacteria per gram dry weight.5.13
The cyanobacteria Hyella ceaspitosa, Plectonema terebrans and Mastigocoleus testarum can occur quite frequently and thrive in the photo-trophic zone (from the intertidal all the way down to 30m and more). At shallow depths though, mechanical parameters become the limiting factors of these microorganisms. In particular, surge and wave action hinders microbial settlement unless sheltered and protected areas enable them to perform their regular activities. In wave-battered areas such as the reef crest, microbial activity is usually limited to species such as H.caespitosa. It can only thrive under such conditions by etching out little depressions and thereby penetrating the substrate to fully unfold its bioerosive properties (fig.5.2).

 


Fig.5.2: Sketch of Endolithic Cyanobacteria (90kB) 5.14

Fig.5.3: Endolithic Cyanobacteria (155kB) 5.15

As mentioned in the previous chapter, mixotrophic cyanobacterial species such as Oscillatoria spp. encroach upon the surface of coral, to feed both on the MPSL while at the same time performing photosynthesis. Current understanding suggests that their metabolites may be toxic to coral tissue; e.g. O.submembranacea may cause or be a component of band-type necrosis in stressed or injured corals.5.16

Kingdom PROTISTA
The most commonly recognized single celled eukaryotic organisms in reef-ecosystems are foraminifers. With regard to coral health and disease, these benthic (some epizootic others epiphytic) are harmless but important contributors to carbonate accretion and quite important in the overall carbonate turnover. However, other members of this kingdom have been found to affect coral health in an adverse manner; in particular some microparasites commonly found within the microbial loop, namely protista, coccideans, ciliates and amoebozoa (that may play a yet unknown role in the calicoblastic epithelium of Siderastrea spp.).

Skeleton Eroding Band (SEB) was first documented in PNG (1988) and has since been observed across the Indo-Pacific from the GBR to the Red Sea. So far no occurrences have been reported from the Caribbean. This disease is caused by the ciliate Halofolliculina corallasia (class Polyhymenophorea) and affects 24 scleractinian species among Pocilloporidae, Faviidae, Poritidae, Fungiidae and Merulinidae but is particularly common among Acroporidae. This sessile folliculinid heterotrich secretes a black sack-shaped test (lorica), which is embedded in the host coral skeleton. Batteries of this ciliate form dense clusters and forms a characteristic black band (fig.5.4).



Fig.5.4: Skeleton eroding Band (125kB) 5.20

Progression of SEB across the coral colony occurs asexually, whereby larval stages move en-mass towards nearby healthy tissue where they settle and secrete loricae. Thus, the band migrates at a rate that may be as slow as 1mm per week or as fast as 1mm per day and leaves a dead skeleton in its wake. Death of the living tissue is achieved chemically via etching activity associated with the production of pseudo-chitinous loricae. The same process is involved when the basal region of the loricae is deposited into the coral skeleton.
Unlike BBD (presented in Chapter-IV), in SEB-affected colonies there is no microbial mat that can be easily lifted from the coral surface. Furthermore, the denuded skeleton is flecked with tiny black spots composed of clusters of empty dark-pigmented loricae, rather than a bright white skeleton as with BBD-affected corals (see fig.5.4). Since there is little information about whether the disease is stable or increasing on a reef, the etching pattern produced by SEB holds promise that this disease might also be found in the fossil record. Hence, it could possibly be used as a proxy for the frequency of other coral diseases and might shed light on the complex question of whether coral diseases are unusually common in the present ocean or whether they can also be found in comparable frequency in the fossil record.5.17 SEB is most common at 0.5 to 3m but is also found at depths up to 35m and seems not to be correlated with seasonal changes in seawater temperatures. Given the limited motility of the larvae, SEB can only be transmitted from a diseased colony to a healthy colony via direct physical contact. Attempts to transmit the disease via seawater in enclosed aquaria were unsuccessful.5.18

Sporozoa: are strictly parasitic protists, which includes the genus Plasmodium, the parasite responsible for malaria. Like all spore-forming protists, Nematopsis is one of those parasitic members that may be responsible for hypertrophy in Porites spp. colonies (see tumors, Chapter-IV). Another sporozoan that is grouped in the phylum the Apicomplexa, subclass Coccidia (an order in the subclass Telosporidia) is Gemmocystis cylindrus, believed to affect Porites astreoides, a commonly occurring coral of the Caribbean. It has been observed to regularly bleach in the fall of every year only to recover later on. Histopathological examination revealed that bleached tissues were devoid of endosymbionts, but otherwise still in good condition. However, in many areas of the gastrodermis both oocysts and released sporozoans of G.cylindrus could be found.5.21 It is still not known whether this coccid is the cause of bleaching or were there is something about its life cycle resulting in temporary displacement of the endosymbionts only to recover once the parasite has been discharged.


 

Fig.5.5: Sporozoan (125kB) 5.22

Kingdom FUNGI
Since fungi are predominantly saprophytic organisms, their presence in the marine environment covers the range from the lower intertidal all the way down to abyssal depths of the oceans. So far twelve genera belonging to Deuteromycota (Fungi imperfecti) have been isolated from a variety of scleractinian corals and a hydrocoral. Their hyphae penetrate into the carbonate matrix by etching narrow canals thereby penetrating deeply into coral skeleton.5.23a


 

Fig.5.6: Fungal hyphae (160kB) 5.23b

Since fungi actively etch calcareous surfaces, they weaken the overall compactness by dissolution of calcareous sediments, as well as the calcareous tube linings of various epiliths and endoliths. Some Ascomycetes such as Lulworthia kniepii infiltrate the calcareous rhodophytes Lithophyllum, Pseudolithophyllum and Porolithon. It probably feeds on the middle lamellae rather than the calcified cell walls of the host.5.24
The following two examples illustrate the degenerative properties on Alconacea (soft corals) and Scleractinia (hard corals).

Aspergillosis (ASP) is a well-characterized fungal infection. This kind of epizoism is caused by Aspergillus sydowii, a terrestrial fungus with a worldwide distribution. Upon infection, Gorgonian colonies may lose tissue, and ultimately, mortality may occur if the infection is not sequestered. The fungus first causes the recession of the coenenchyme (the recessing living rind tissue exposes the urple sclerites giving the lesions a purple halo fig.5.7a) and thereby exposing the internal axial skeleton (central protein core). The mechanisms by which A.sydowii produces tissue degradation and nodule formation is still unknown, but virulence of the pathogen increases with elevated seawater temperatures (i.e. 30C). Upon contact with a potential host A.sydowii germinates to infect it. Thus, hyphae (not spores) must break free from an infected gorgonian and reach the surface of the water to produce spores.
Secondary transmission of ASP from infected to uninfected sea fans may occur through (1) direct physical contact with an infected individual, i.e. a diseased sea fan may brush against a close neighbor, (2) transport of fungal hyphae in the water column, or (3) transport of fungal spores (produced at the sea surface from hyphae released from diseased sea fans) in the water column.5.25
It is interesting to note that A.sydowii is a terrestrial fungus, which can be easily introduced into the marine environment either with local sediment runoff or via long distance transport. The spores of A.sydowii are small enough (<5m) and are easily picked up by winds and dispersed over great distances (fig.5.7). Whereas if local runoff is the source, then ASP most likely is linked to anthropogenic disturbances. So far marine currents seem not to contribute to the spread of ASP over larger distances. Since ASP as a terrestrial fungus has adapted to the marine environment, it appears that both mechanisms are plausible, with local anthropogenic contributions and dust storms originating in Africa alike act synergistically.5.26

 


Fig.5.7a: ASP on sea fan (120kB) 5.27

Fig.5.7b: Sahara dust storm (120kB) 5.28

In addition to Gorgonia ventalina and G.flabellum, ASP has also been observed on 6 other gorgonian species across 5 genera (i.e. Pseudoterogorgia americana, Gorgonia mariae, Plexaura flexuosa, Pseudoplexaura porosa and Plexaurella nutans). Although it primarily affects Octocorallia, particularly Gorgoniidae (Gorgonia ventalina and G.flabellum), it is also capable to bioerode living stony corals (interaction between polyps and fungi causes pearl-like skeleton bio-minerlaization - see below, FI).5.29 However, Kochs postulates in establishing A.sydowii as the causative agent have only been fulfilled for G.ventalina and G.flabellum.

Other Fungal Infection (FI) on scleractinian corals: the syndrome largely affects Astreopora, Montipora and Echinopora, and to some extent Acropora, Goniopora, Platygyra as well as massive Porites (fig.5.8a). In its early stage, diseased corals develop an ashy dull coloration with a brittle or weak skeleton while in the intermediate stages they become covered with mucus and this collects debris. Once the mucus and debris clears, a white calcareous dust is left on the surface and at times a black layer is formed underneath (probably due to anaerobic microbial decay of the tissue under the mucus). Death is very quick and occurs in less than 2 weeks.5.30


 

Fig.5.8a: Fungal Infection (90kB) 5.31

The syndrome on branching species can hardly be confused with abiotically-induced coral bleaching; it only affects a few taxa (Echinopora & Astreopora-species are quite resistant to this kind of bleaching) and with dull tissue coloration that does not attract too much attention. Bleaching of some massive and submassive species however, is often protracted taking weeks to months to die and is accompanied by vibrant color changes. Unlike commonly reported microbial diseases that form bands, there is no band formation, just an ashy texture or loss of color.5.32 The mycelium of the fungi Scolecobasidium sp. is known to affect several coral species along the coast of the Bay of Bengal. It forms a conspicuous and dense brown to black zone (5-15mm in width) underneath the coral surface, while the coral reveals the fungal presence by necrotic patches that can affect up to 50% of the colony.5.33 It was observed that among the massive corals Porites lobata of French Polynesia, tiny protuberances decorate the surface of the colony, which were found to contain hyphae of endolithic fungi. The coral polyp itself responds by shutting off hyphaeal access by increased carbonate accretion. As long as the colony is capable to do so (i.e. request to be in good health) the fungi is more or less trapped within the carbonate cage.5.34a

Part of the pathology associated with PLS (Pink Line Syndrome, briefly described in Chapter-VI), is probably related to an unidentified hyaline, non-sporulating fungi (HNS), a mycelial fungus identified as Curvularia lunata and an opportunistic dark, non-sporulating fungus (DNS). Like ASP, most identified fungal strains belong to terrestrial genera. Nonetheless, these fungi are also found in corals devoid of any symptoms, although the highest fungal frequency is found in the dead patches of PSL-affected coral colonies, in which DNS prevail with 60% over 30% of HNS strains (compare fig.4.9c Chapter-IV).5.34b Since non-sporulating forms are quite common in corals, it further indicates that these fungi survive and propagate via hyphal fragments rather then by spore formation (fig.5.8b).


 

Fig.5.8b: PSL-affected Porites lutea (130kB) 5.34c

As with the former (i.e. fungal infection such as ASP), tissue invasion can either take place by a foreign fungus possibly associated with the water mass or an endolithic taxa feeding on coral tissue that died from other means (either another disease or unfavorable abiotic conditions during a given season). Yet another working hypothesis assigns the fungal hyphae a more opportunistic role; i.e. after exposure to external stressors, the ever-present and co-existing endolithic fungus (associated with the coral host) tipped in favor of the fungus. Under such circumstances the fungus are able to invade the coral tissue without the usually effective defense response from the coral. In a healthy coral the colony typically responds by increased calcification over the pore created by the hyphae (nob-like protuberances leaving only a few pores that indicate penetration into the coral tissue). Under such circumstances the death of the colony may be the result from a local imbalance in the coral-fungus relationship - a hypothesis, which explains the rapid death of coral colonies, the uniform distribution in reefs, and the simultaneous dis/appearance of this syndrome in disparate reefs.5.35a
Although certain obligate marine fungi have been described in coral slab, less important facultative marine fungi of terrestrial origin have been isolated from corals alike.5.35b Yet, it seems that corals have "learned" to deal with most of them. However, the finely tuned dynamic equilibrium among species and the lowered host resistance of key species (i.e. corals) due to stress-related factors has assigned some fungi increased pathogenic properties.

Kingdom PLANTAE
Green (chlorophyta) and red (rhodophyta) algae are implicated in the erosion of rock and biologically deposited carbonate substrate. So far green and red algae have only been observed on limestone surfaces (epilithic especially during inter-specific competition), in cavities and crevices (chasmolithic niche specialization), and within coral skeletons (endolithic). While excessive epizootic growth of filamentous algae smothers and shades coral tissue, colony death can be triggered by excessive endolithic activity resulting in a weakened skeleton no longer capable to withstand mechanical stress.

Algal Galls (GALL): Opportunistic infection by the microalgal species Entocladia endozoica (Chlorophyta) is known to affect the skeleton of gorgonian corals (genus Pseudoplexaura) across the Caribbean. The host tissue reacts to the presence of algal filaments by producing a capsule composed primarily of an accumulation of scleroprotein skeleton (gorgonin) and calcareous sclerites. The skeletal capsule separates the algae from contact with host tissue, but in doing so the skeleton loses more than 60% of its tensile strength and over 90% of its elasticity (fig.5.9). The coral colony readily breaks apart at the site of the infection, exposing the algae to relatively high light levels and seawater. Being exposed to a sudden illuminated and amino acid-depleted environment, triggers rapid cytological changes within the algal filaments, thereby stimulating the development of reproductive structures containing gametes. Regeneration of damaged host tissue (coenchyme of the coral) re-seals the capsule and causes resumption of the vegetative condition typical of the enclosed algae. Experiments with native and cultured material suggest that host-derived amino acids, especially tyrosine or cystine, play a key role in regulating the reproductive condition of Entocladia filaments.5.36a

 


Fig.5.9: Allgal Galls (115kB) 5.36b

Endolithic band formation: Freshly fractured corals often reveal layers of green banding a few centimeters beneath the live coral surface. The green pigmentation results from chlorophyll, used by the algae to intercept light passing through the coral's tissues and skeleton (e.g. Ostreobium spp. band). The ubiquitous boring algae Ostreobium quekettii often lives in association with fungi and within the skeleton of stony corals - just a few centimetres below the surface (fig.5.10). It forms thalli (2-5m in diameter) that develop on the surface and gradually make its way into the occupied substrate. It optimises the photo-autotrophic efficiency by using the thalli like "fibre-optical cables" (compare fig.5.2).5.37 Due to shading properties of the carbonate and MPS-layer above, light becomes the limiting factor. Although Ostreobium develops when the growth conditions for the coral are optimal, this endolithic autotrophs experience accelerated cycles of growth especially when grazers remove the uppermost layer of the substratum (whereby photosynthesis exceeds the compensation point of cellular respiration).

Similar boost of algal growth does also occur when the coral is stressed, thereby exacerbating recession and allowing other opportunistic species to bring about disease and tissue necrosis.5.38 Furthermore, turbidity of the water column can limit the presence of this endolithic algae to the photo-trophic zone. The greenish layer often observed in freshly fractured corals is not always an Ostreobium band, but can also be comprised of several genera of algae; i.e. Codiolum, Entocladia, Eugomontia and Phaeophila.5.39 However, the importance of these endolithic bioeroders is still controversial. Yet it is assumed that a healthy colony tolerates endolithic activity, while a disturbed host exerts a positive feedback onto the inflora, thereby stimulating its endolithic activity. Some rhodophyta such as Plocamium hamatum frequently grow on soft corals, especially Sinularia spp. (Alcyoniidae). This alga releases a terpene, known as chloromertensine that can kill its host.
The dinoflagellate Cochlodinium catenatum has been reported to cause coral bleaching and tissue sloughing with Tubastraea sp. and Pocillopora sp. among the most affected. Gonyaulax monilata a member that is also responsible for "phosphorescence of the sea" is another toxic dinoflagellate that can induce coral mortality.5.41

 


Fig.5.10: Ostreobium band (205kB) 5.40

Algal Epizoism: The roughness of the waters, (due to sea-level variations, tides, currents and swells) forces organisms to adapt. Such hydrodynamic effects select species like the encrusting phaeophyte Lobophora variegata or calcified species such as corallinacean rhodophytes.5.42c However, far more invasive are the following corallinacean rhodophytes:
Pneophyllum conicum (PNE): A totally different way to outcompete coral resilience is used by this coralline red algae. P.conicum was first documented in the Southern Indian Ocean, and later-on observed to be widespread across the Indo-Pacific. PNE simply overgrows and kills live coral.5.42a On Mauritius, this pattern of epizootic growth affected up to 80% of the corals on one particular reef-crest (fig.5.11b). Many large corals were totally enveloped by two, three or more contiguous thalli, some measuring almost 1m in diameter. In comparison and during a previous reef health survey in Mauritius in 1990, no PNE was registered. Once PNE is established on the colony, mortality levels regularly reach 100%.5.43 Epizoism on scleractinian by P.conicum in such radical manner appears to be another manifestation of the ongoing global shift in reef dynamics. A very similar syndrome PEY has recently been discovered in the Caribbean (see next).
Meta-Peyssonnelia (PEY): Another encrusting rhodophyte is caused by this unusual Metapeyssonnelia corallepida. This is a recently identified and documented epizootic red alga from the Caribbean. So far this species was only known to occur in the Mediterranean Sea, and was neither documented on reef surveys dating back as far as 1975, nor described outside its original habitat. It starts to grow at the dead base of coral colonies and from there proceeds upwards overgrowing and destroying living polyps and the coenosarc.5.44 PEY overgrows entire coral colonies such as the typical reef-crest hydrocoral Millepora complanata (fig.5.12) and M.alcicornis as well as scleractinian corals such as Porites porites and P.astreoides. In doing so, M.corallepida forms a tightly attached algal "skin", which covers the coral surface. The density of the algal mat is so intense that the underlying living coral tissue gradually suffocates, thus leaving no trace of coral tissue.


Fig.5.11a: Coralline Algal overgrowth (330B) 5.41b

Fig.5.11b: Pneophyllum conicum (125B) 5.42b
 

Fig.5.12: Meta-Peyssonnelia (185B) 5.45

Kingdom ANIMALIA
Once higher animal taxa are involved in bioerosive processes, the spectrum of inter-specific competition between coral species and other animal taxa becomes particularly vivid. With substrate being scarce competition among sessile organisms is particularly fierce and an essential part of the dynamic balance in territorial gain. Since corals are at the very center of reef dynamics, it comes of no surprise that a myriad of heterotrophic species is feeding on almost anything the coral animal provides among them are endolithic sponges, corallivorous snails, starfish and herbivorous parrotfish, which give excellent examples.

Porifera:
Sponges are perceived to have only a minor structural role in living coral reefs. Apart from some importance in accreting coral skeleton in deeper waters and some autotrophic sponge communities (with endosymbotic cyanobacteria), "boring, burrowing and encrusting" sponges are found on most coral reefs.5.46 Their abundance can drastically increase under eutrophicated conditions, thereby negatively influencing the dynamic equilibrium towards filter feeders such as sponges (see eutrophication, Chapter-III). Endolithic sponges actively etch calcitic and aragonitic substrates including live corals notably members of siliceous sponges (class Demospongiae) are known to include bioeroders and are found within the order Hadromerida, (Terpios, Spirastrella, Cliona, Chondrilla, Anthosigmella, and Spheciospongia) as well as within the order Haplosclerida ( Siphonodictyon).5.47 Here, sponges of the family Clionidae are found on coral reefs worldwide, are the most common and destructive endolithic bioeroders.

Cliona sp. possesses specialized "scraper" cells (amoebocytes) that etch their way into the calcareous substrata and chip minute fragments from limestone rock or precipitated coral skeleton (especially within Pocilloporidae and Poritidae). Enzymes dissolve the calcium carbonate skeleton (along with any organic matter), while fine pseudopodial (filopodia) sheets are extended into the etched canals, flatten out against the calcareous substratum and coalescence centrally, resulting in a hemispherical carbonate chip to be broken free from the substrate (fig.5.13). Altogether only about 2-3% of coral skeletons are dissolved chemically, the reminder is extracted as silt-sized chips.5.48 At the end of this process, both chips and etching cells are transported away and expelled trough the sponges osculum.
Depending on the coral species and infestation density of C.lampa, it is capable of eroding CaCO3 substrate at a rate of 10-80mm per year (which amounts to approx. 23kg×m-2×a-1) and thereby contributing significantly to the coral slick fraction. It is estimated that 30-40% of reef sediment has its origin in endolitchic sponge activity. Thus, any ecosystemic imbalance that may favor endolithic activity by boring sponges (such as eutrophication), excerts detrimental effects on the overall carbonate accretion and the corresponding sediment production. Since it does not harm living tissue, affected corals are weakened structurally, i.e. less capable of withstanding mechanical stress. Fast growing species are thus experiencing mechanical fragmentation and able to asexual reproduction.5.49


 

Fig.5.13a: Endolithic sponge (105kB) 5.50

Fig.5.13b: Etching activity excerted by C.lampa (100kB) 5.51

Spongal Epizoism: Sponges can also be problematic in that they are very prolific in their secretion of allelopathic substances and other chemical compounds, and these may have an indirect effect in preventing coral growth or colonization. Members of the class Demospongiae such as Aplysilla spp. are usually encrusting, with great reduction in their fibrious skeleton. These sponges lack spicules and rely on dendritic fibers for skeletal support (fig.5.14). The encrusting sponges Spongia tubulifera, Aplysina fistularis and Ircinia felix are also known epozootic species with detrimental effects on corals. Likewise does Plakortis halichondrioides kill and overgrow all tested corals upon contact and near contact, including bleaching, necrosis, and coral tissue lysis.5.52 Sponges of the genus Siphonodictyon spp. and many others alike, secrete mucus-borne metabolites, siphonodictyal and siphonodictidine, which directly kill nearby coral polyps, even increasing coral respiration rates from some distance away.5.53 Typically seen are decreases in photosynthesis and increases in oxygen consumption/respiration in corals with sponges nearby.
 
Terpios hoshinota is grouped in the family Suberitidae (order Hadromerida) and is found across the central to western Pacific. It is recognized by its extensive grayish to blackish encrustation on coral. The sponge aggressively overgrows live coral and causes large-scale reef-damage, particularly in pollution-stressed zones near shore. The intercellular zoocyanellae make up half or more of the sponge tissue. Their morphology, as determined by electron microscope observations, is identical to that of symbionts described from two species of an unrelated sponge genus from the Caribbean Dictyonella.5.54b

 


Fig.5.14a: Spongal epizoism (155kB) 5.54a
 

Fig.5.14b: Terpios hoshinota overgrowing a Porites colony (205kB) 5.54c

Cnidaria:
Interspecific competition (among various coral species) is a known occurrence among a few corals. During nighttimes, when most corals are actively "fishing" for plankton, territoriality and aggressive behavior is used to increase space for future colony expansion. Some corals like Galaxea, Euphyllia, Goniopora, most mussids and the free-living fungiids, are especially aggressive towards other species within their reach.5.55a By extruding mesenteric filaments they are able to digest the living tissues of surrounding neighbours.

Other species use sweeper tentacles, specialized and elongated tentacles to sting other colonies nearby (fig.5.15a). Both extrapharyngal digestion by mesenteric filaments as well as stinging by sweeper tentacles result in denuded interfacial areas on the attacked coral colonies. In some cases even a pecking order can be established; i.e. solitary corals outcompete massive colonial and fast growing branching species, while aggressive ability enables slower growing species to maintain living space (fig.5.15b). In the competition for space aggressive out- and overgrowth is another way to increase colony size. Slow-growing massive corals like faviids and most poritids are easily overgrown by faster growing species. On the other hand, such slow-growing species do more readily resist mechanic disturbances (originating from storm, predation, or bioeroding activity).


 

Fig.5.15a: Use of sweeper tentacles (120kB) 5.55b
 

Fig.5.15b: Interspecific competition among corals (180kB) 5.55c

Turbellaria & Trematodes:
Flatworms are very common in the wild, and their presence is ubiquitous on some reefs and on some species. Some turbellarians are parasitic to corals, though most are commensal. Other flatworms may be found primarily on soft corals (e.g. sea pens have been noted to be affected by trematodes of a yet unknown species). Although little is known about there feeding preferences, some do prey on ascidians, while others are suspected that some corallivors species are among the genera Pseudoceros spp. (P.sapphirinus on Acropora), P.zebra, Paraplanocera spp. and Stylochoplana spp.5.56 Upon contact with branching Porites colonies, cercaria of Plagiosporous sp. use their suckers to attach itself to the living coral tissue, cast off their tails, and within minutes have digested their way through the upper ectodermis. They then encyst to their secondary intermediate host as a metacercaria, a stage which can remain alive and infective for months or even years.5.57 Encysted within the soft tissue of the coral they form 3-5mm cysts some 1-2mm high that can cover the entire coral surface when present in high enough numbers. This is a true parasitic stage of this worm, but although there is some local damage that occurs with such infestations, even those colonies covered heavily with cysts are generally tolerant and do not die from their presence.5.58

Pink Spot Disease is caused by the larval stage of the parasitic flatworm Podocotyloides stenometra and has only recently been recorded on the Great Barrier Reef (around Lizard Island and No Name Reef at the northern GBR). The flatworm has three life stages: the first is parasitic on a mollusc, while the second affects tissues of the coral Porites compressa, causing polyps to appear swollen and pink. This makes the polyp more vulnerable to predation by butterfly fish, which are the final host for the parasite. Once the infected polyp has been eaten by the butterfly fish, healthy polyps regenerate from the coral.5.59a Since most trematods are parasitic even to many higher animal taxa (including humans, e.g. liver fluke Clonorchis cinensis), it is not surprising that these parasites use the soft coral tissue in partial fulfillment of their life cycle.


 

Fig.5.16: PSD (120kB) 5.59b

Mollusca:
Bio-erosion by molluscs occurs either by mainly mechanical or chemical means (except for some predatory gastropods, e.g., Naticidae, where both means may be of equal importance).

  • External erosion, through abrasion by grazing chitons and gastropods has its main effect in the inter-tidal (with a substantial contribution to the building of a coastal notch in limestone and reef habitats). Further, these molluscs cause very little external erosion by dissolution of the substratum at their resting places (and even less below attached egg capsules).
  • Internal erosion by molluscs is restricted to boring bivalves and a few coralliophilid (and possibly vermetid) gastropods. Octopod cephalopods, preying on bivalves and gastropods and thus producing bite marks on and boreholes in the shells of their prey, cause minimal bio-erosion by mechanical respectively chemical means.

Chitonidae are potential abraders of intertidal limestone. Using their Magnetite reinforced radula, they contribute to the development of a coastal notch. Erosion rates for Acanthopleura spp., growing about 30-40mma-1, amounted 0.45-0.61 mma-1 at Aldabra Atoll in the Indian Ocean and 0.7mma-1 at Heron Island, GBR 5.60. A.brevispinosa from Aldabra Atoll, with a mean population density of 4.8m-2 and mean size of 36mm, produce 40.2 gm-2a-1 and even under a maximum density of 11m-2, the erosion amounts only 0.038mma-1.5.61 Erosion by A.granulata was estimated to amount 0.21 mma-1 on Caribbean Andros Island,5.62 and 0.12 mma-1 at San Salvador, Bahamas.5.63 In the Caribbean shallow subtidal, Choneplax lata, feeding primarily on corallinacean Porolithon pachydermum, induces a mean accretion of 2.3mma-1. A similar situation is found on Astrolabe Reef, Fiji, by Porolithon onkodes and Chryptoplax larvaeformis.5.64 In the intra-to supra-tidal, various gastropods (e.g., Littorina, Nerita, Cittarium on beachrock) contribute to coastal erosion, by rasping with their radula epi- and endolithic algae from the limy substrate. Thus, accelerating bio-erosion by microboring cyanophytes. Patella populations of 10-15m-2 erode 1.5mma-1.5.65 Depending on the zonation and population density of the animals, bio-erosion amounts between 0.1-1.1mma-2 in the northern Adriatic.5.66a

 

 


Fig.5.17: Chiton on Rock (135kB) 5.76q

Boring gastropods, e.g. Leptoconus, associated with certain live scleractinian host corals are of more biological than bioerosional interest. Other Coralliophilidae use corals only as food, e.g. Coralliophila or Drupella.

The prosobranch gastropods in the families Architectonicidae (sundials), Epittoniidae (wentletraps), Ovulidae (cowries), Muricidae (murex), and Coralliophilidae ("coral lovers") consists of the rapa and coral snails are the most likely to prey on corals. Muricidae (Murex and Coral snails): members within this family include well-known coral predators. Coral tissue is rasped off with their radula. Since they can reach extremely high population densities these are considered major coral predators, possibly second only to Acanthaster planci.5.66d The genus Drupella includes at least four species, D.cornus, D.elata, D.fragum, and D.rugosa that have been shown to cause extensive reef damage in areas where their densities have reached outbreak dimensions. Aggregations tended to be found in areas with high cover of acroporid corals. Species of this genus appear to be generalist corallivores, although some studies have suggested preferences to other corals. D.cornus for example is a notorious corallivore and preferably rasps on tissues of Porites spp., Stylophora spp., Seriatopora spp., branching corals, Montipora spp., Acropora spp., Pocillopora spp., Echinopora spp. and Porites compressa (fig.5.18). D.rugosa prefers Acropora spp and Pocilloporidae. In outbreak densities, predation by these species typically results in 95% tissue loss on live corals. Such population outbreaks are not just the result of natural fluctuations but are likely linked to anthropogenic influences that either reduce mortality of the larval stage of Drupella spp (due to overfishing of snail predators) or through increased runoff and siltation (as a consequence of altered coastal environments).,

There appears to be a strong correlation between the abundance of snails and the prevalence of diseases. During that reef survey in 1996 (Ras umm Sidd near Sharm el Sheikh, Gulf of Aqaba), corals were found to suffer from a deadly combination of a D.cornus population explosion and an epidemic outbreak of White Syndromes (a spectrum of coral diseases involving WBD, WPX, WPL and SDR - see Chapter IV).5.66e It is still not clear, however, if massive coral die-offs (mostly due to WS) attract or benefit D.cornus, or whether a population explosion of D.cornus promoted an epidemic of WS among the corals.5.66f

Since Coralliophila species lack the radula they use salival enzymes to suck the externally dissolved coral pap. Affected coral tissues treated in this way rarely recover, as filamentous algae are generally the faster colonizers of such denuded substrate.
C.violacea is a sessile snail that remains on its host coral where it produces a thin aragonite attachment layer and only moves to feed on nearby tissue of Porites spp., Pocilloporidae and Acroporidae. C.costularis migrates from coral to coral, but stays near the centremost branches for protection; it moves outward when devouring living tissue of branching Porites spp., Pocilloporidae and Goniopora spp. C.caribea preys on gorgonians, A.palmata and D.clivosa. C.erosa feeds on Acropora spp. and Montipora spp. C.sugimotonis on Palythoa spp. (anthozoa).5.66g C.abbreviata is found on Montastrea annularis, Acropora palmata, Diploria clivosa, and Favia fragum (fig.5.19). In the Caribbean, C.abbreviata was found on up to 64% of coral colonies and was associated with coral mortality off stressed colonies.5.66h


Fig.5.18a: Drupella on Acropora (90kB) 5.66f
 

Fig.5.18b: Epitonium feeding on Tubastraea (175kB) 5.76r
 

Fig.5.18c: Coralliophila on Acropora & Porites (120kB) 5.76rr

Boring bivalves have developed in nine families distributed in five orders in three subclasses: Pteriomorphia (Arcoida: Arcidae; Mytiloida: Mytilidae), Heterodonta (Myoida: Gastrochaenidae, Hiatellidae, Myidae, Pholadidae, Teredinidae; Veneroida: Tridacnidae, Petricolidae) and Anomalodesmata (Pholadomyoida: Clavagellidae).5.66b (for taxonomic position of boring bivalves, see note).5.66c

Chemical borers include (for mechanical borers, see below):

  • all Gastrochaenidae (Eufistulana, Gastrochaena including Cucurbitula, Spengleria, and extinct Kummelia) and
  • mytilid Lithophaginae (Lithophaga, Leiosolenus, Botula, Fungiacava, and probably except some Adula species),
  • further some Crenellinae, Gregariella coralliophaga and G.coarctata, Pholadomyoida, Clavagella (Bryopa) lata, and a
  • few Pholadoidea, e.g. Penitella conradi, Jouannetia cumingii, Tridacnacea, Tridacna crocea, Veneroida, Petricola lapicida, P.lithophaga, and P.hemprichi, Petricolidae), and probably Hiatella arctica, Hiatelloidea, and Platyodon cancellatus, Myoidea.
  • Others are facultative borers, e.g. upper Ordovician Corallidomus scobina and recent pectinid Pedum spondyloideum. Indications for chemical boring in limy substratum are bilateral symmetrical boreholes, traces of dissolution on the walls, flaring orifices, borehole parts out of shell reach.

 

 


Fig.5.19a: Pedum in Porites (175kB) 5.76s

Lithophaginae, mainly tropical and sub-tropical in distribution, except Mediterranean Lithophaga lithophaga (reaching at least 54 years of age), are generally etching into calcareous substrates for shelter. The process is performed by byssal attachment as holdfast and long lasting contact of the mantle and siphon tissues with the substratum, which is (at least partly) dissolved by secretions of the epithelium or more or less specialised, so-called boring glands. Dissolution acts primarily on the crystal connections (in coral) or the matrix between grains (in limestone and rock with calcareous components) and must not be complete. Loosened particles are expelled as pseudo-faeces. According to the main boring direction and shell form, the necessary protrusion and reflection of the mantle over the shell is performed primarily at the anterior and usually less ventro-laterally, except in somewhat heart-shaped Fungiacava, where the shell is almost completely enveloped to enable widening of the characteristic dwelling. The latter encases the smooth and fragile shell closely, indicating the almost complete inhibition of shell movements, being restricted to closing and opening them a little. No rotation within the borehole is possible.

Species of sub-cylindrical, ellipsoidal Lithophaga s.s. have fine elevated lines perpendicular to the antero-ventral shell margin and lack any species-specific calcareous shell encrustation. The largest species, L.antillarum (largest specimen measuring 145.036.5-29.4mm), shows an additional criss-cross pattern of elevated lines on the postero-dorsal shell surface. Species-specific shell encrustations are a characteristic feature of Leiosolenus, of which eastern Pacific L.attenuatus is the largest ahead of inflated L.obesus. Most species of Lithophaga and Leiosolenus bore in dead coral, but some of the latter have developed an obligate association with certain live scleractinian host corals,5.67 except Caribbean L.bisulcatus, which is also found in dead coral or big shells.5.68 Boring and growth rates of various bivalves, mainly mytilid representatives, from the Caribbean, eastern Pacific and Great Barrier Reef have been found positively correlated with size in general and particularly the nutrient supply, which was highest in the eastern Pacific, culminating in L.attenuatus. The latter showed a boring rate of 0.130mm/d at 49mm borehole depth and a growth rate of 0.084mm/d at 29mm bivalve length. The respective rates for L.aristatus were 0.099mm/d for at 29mm borehole depth and 0.058mm/d at 21mm shell length. Maximum boring and growth rate in Caribbean L.antillarum was 0.071 and 0.033mm/d respectively.5.69 Small sized Fungiacava eilatensis, sole species of the genus and a maximum size of 15mm in length, is associated with live fungiid coral.5.70 Living ventral side up, the siphons open into the coelenteron of the host. The rather bean-shaped, up to 40mm long and quite robust shells of Botula, are smooth, lacking any own encrustation, and have a relatively thick periostracum, a concave ventral outline and prominent terminal beacks, being sub-terminal in the other genera. Maximum boring and growth rate in Caribbean Botula was 0.040 and 0.012mm/d respectively. Some Adula species are reported mechanical borers, but lack any suitable shell morphology for it.5.71 Generally, boring direction in Lithophaginae is perpendicular to the substratum surface but may be altered due to environmental factors. Under crowded conditions even intra-specific space competition occurs. While the elongated shells of Lithophaga and Leiosolenus hinder an easy shift in boring direction, some Gastrochaena with long siphons are capable to avoid cutting into neighbouring borings. Particularly Lithophaga boreholes have been used as indicators of previous sea level horizons.

 

 


Fig.5.19b: Fungiacava in Fungia sp. (85kB) 5.76t
 
 
 
Fig.5.20a: Lithophaga in Porites sp. (240kB) 5.76u
 
 
 
Fig.5.20b: Lithophaga coralline infauna. (120kB) 5.76v

Crenellinae have at least two chemically boring species, Gregariella coralliophaga and G.coarctata, of which the latter has much faster boring and growth rates, requiring little more than two years to reach an outgrown size of 20mm, while the other needs more than ten years.5.72 Borehole shape resembles the characteristic shell with a somewhat triangular median cross-section.

Gastrochaenidae, mainly tropical and sub-tropical in distribution, except temperate Gastrochaena dubia, are altogether able to dissolve calcareous matter as well as to line their dwellings, particularly the siphonal parts. Laking a byssus, the foot, functioning as suction disc, acts as a holdfast and pivot during boring activity, sometimes leaving a slightly elevated mark on the borehole wall. The ability to dissolve calcareous substrates is obvious in boring Spengleria and Gastrochaena, to a lesser extent in tube building and inhabiting Eufistulana, except when the tube in the surrounding fine sediment cuts a shell in its way and penetrates straight forward. Spengleria, which has an antero-vetrally gaping shell like Gastrochaena, has its siphons separated in v-shape, and thus the boring opens in two separated, circular holes. The siphons of Gastrochaena are connected and line their borehole walls, opening in a figure-of-eight, sometimes clearly elevated above the surface like chimneys. The small G.(Cucurbitula) cymbium settles on shell debris and, after penetration, builds iglu-tubes to encase itself.5.73a

From Clavagellidae, so-called watering can bivalves, only species of Clavagella (Bryopa) are producing boreholes and, as the left valve is cemented to the substratum, obviously by chemical means. C.(B.) lata is probably the sole species with a number of junior synonyms.

Arcoid Litharca lithodomus, is the most peculiar species of recent Arcoidae as it is the only one with a rock-boring habit.5.73b The shell is smooth, anteriorly attenuated, with a weak ligament, and the umbos lying far back from the anterior extremity. Boring is obtained most likely by solution as in Lithophaginae,5.73c which can be concluded from shell shape and sculpture,5.73d although other authors consider mechanical boring as more likely.5.73e Geographically, the species is restricted to the NW coast of South America, from Manta, Ecuador, to Cabo Blanco, Peru, with a questionable occurrence at Panama, occupying rock and boulders in the inter-tidal.

Myidae: Platyodon cancellatus, bores [burrows] mechanically with ribbed shells (sculptured with regular, fine concentric lines) into mudstone, hard clay and soft stone [heavy clay or soft shale of bays and estuaries] of the inter-tidal and grows to 7cm in length. The siphons have two pairs of pointed plates near their tips.5.73f

Hiatellidae: Hiatella arctica is reported to have a mean boring rate of 0.67cm/a for three-year-old specimens and 0.5cm/a for eight year ones. It ranges from 0.125-1.0cm in lenght.5.73g The shell is oblong in shape but highly irregular with no two specimen being alike. Thus, the species may be primarily nestling and only facultatively boring. It is estimated the mean growth rate to amount 0.14mm/a with a maximal size of about 37mm, which may be reached within 35 years.5.73h

Tridacnidae include three chemically boring species in Tridacna (Chametrachea). T.(C.) crocea is sunken ventral side up into dead upper parts of coral heads on reef flats, T.(C.) maxima and T.(C.) squamosa, may be partly wedged in between or embedded by live coral, leaving etch-marks at contact zones of mantle tissue and substratum. At the Great Barrier Reef average populations densities of T.crocea (4.4m-2) on interior reef flats were estimated to remove about (60)100cm3 or 140g·m-2a-1 from the leeward reef.5.73i Similarly, other authors noted that pedal (?) mantle tissue recurved upward, often reaching the surface of the boring and completely encasing the posterior end of the shell within.5.73j Nevertheless, they trusted more the mechanical boring hypothesis of Yonge.5.73k



Fig.5.21a: Tridacna in Porites (210kB) 5.76z

Pholadidae: Early juveniles in all pholads employ anterior boring. Later, many pholads continue anterior boring throughout life, whereas others gradually shift toward ventral boring. The latter being a specialized character derived from anterior boring.5.73o Pholadidae (Jurassic to Recent) comprise 4 sub-families:

  • Pholadinae (Cretaceous to Recent, Pholas, Barnea, Cyrtopleura, Zirfaea), shells elongated, without umbonal-ventral sulcus (except Zirfaea), with apophysis and 1-3 additional plates, boring in shale, peat, soft rock, shells. Penitella conradi, although a pholadid, bores by reflecting its mantle over its anterior and thus penetrates the shells of live abalone on the Pacific coast of North America. An almost 20cm long abalone contained 48 specimens. The largest out of 515 was 53mm in length.5.73l



Fig.5.21b: Parapholas in coral rock (100kB) 5.76zz

  • Martesiinae (small wood-boring Martesia, Jurassic to Recent, brackish Lignopholas, shell-boring Diplothyra, dead coral boring Parapholas, Cretaceous to Recent, clay to rock boring Penitella, Miocene to Recent), shells relatively short, with apophysis and 1-3 additional plates (meso-, meta- and hypoplax), adult, non-boring specimens close the antero-ventral gap of the shells with a callum.
  • Jouannetiinae (Cretaceous to Recent, 2 genera) have no apophysis, in the adult, non-boring phase, the right siphonoplax becomes larger than the left, and the callum of the left valve reaches over the right one. Jouannetia cumingii is another chemically boring pholadid.5.73m
  • Xylophaginae (Cretaceous to Recent genera, deep-sea wood-borers Xylophaga, Xyloredo), use the wood as food, like the Teredinidae (except Kuphus). Shells resembling Teredo, lack apophysis and callum, mesoplax small.

Mechanical borers in bivalvia are distinguished in groups according to their differing method in using their shells as tools.
Those living in sediments, which should be called burrowers not borers, scrape with the antero-ventral rim of the valves, lacking a pedal gape, present in rock-borers. The latter have developed more pronounced shell sculptures, needed for substratum abrasion in a sophisticated three-dimensional movement of the valves, tooth by tooth acting as a minute chisel. To accomplish this chiseling, a number of morphological and anatomical features had to be developed, e.g. a dorsal pivot or ball joint instead of a hinge to allow shell movements in all directions, an apophysis, additional plates and antagonistic mussels. The siphons accomplish hydrostatical support in the boring process.
From all the above, it is not astonishing, that chemical borers have the longer geologic record (since the Triassic), than the mechanical borers, of which the oldest are Jurassic in age.
Mechanical borers can be found mainly in Pholadoidea, of which all Teredinidae, pholadid Xylophaginae and some Martesiinae dwell in wood for shelter and, except Martesia, also for food. Other Pholadidae, e.g. Bankia, Pholas, excavate rock or reef substrates, e.g. Parapholas. Veneroid Petricola pholadiformis, elongated and with shell ornamentation, is a mechanical borer.

Teredinidae are wood-borers and have developed a file technique with their specially formed and sculptured shells, adapted foot, and musculature. A second, ventral pivot only allows shell movements around the dorso-ventral axis, the rectangular pedal gape is wide, and rows of minute teeth are specially arranged for the filing process. As the short valves cover only the anterior of the bivalve, it can swing them also sideways in the boring, which otherwise could not be elongated due to a gap of contact at the end.5.73n Their shells are much reduced, covering the anterior extremity of the worm-like animal. So far, 3 wood-boring sub-families are known:

  • Kuphinae, with Kuphus polythalamia as sole recent species.
  • Terediniae are the smallest pholadids and generally have simple pallets, e.g. Teredo (borings ~2mm across) and Lyrodus, both give birth to larvae.
  • Bankiinae have pallets with many segments, e.g. Bankia, Nototeredo
.

Petricolidae have developed some chemical and one mechanical boring species in the genus Petricola, of which the latter is pholadiform. The former are short, oval, with a more rounded anterior and little elongated posterior half. The narrow, bilateral symmetrical boreholes mirror the animal in life position with gaping valves and extended short siphons, thus indicating no rotation but chemical boring by protruding mantle tissue. This was noted in Mediterranean P.lithophaga, who also observed etch-marks on shells.5.73p

Annelida:
The class Polychaeta includes the most conspicuous worms to be found on a reef. Their members bore into rock and can be quite abundant in tropical reef ecosystems. Various species in the following families typically form circular holes 0.5-2mm in diameter that penetrate up to 10cm into the interiors of coral skeletons: in particular members of Cirratulidae, Eunicidae, Sabellidae, and Spionidae. The following mechanism of boring has been reported for few polychaete species. Most eunicids are herbivores, carnivores or scavengers and employ their mandibles to excavate, thus some are frequently found to bore into dead coral substrates as well.5.73 As with endolithic sponges, spionids are likewise significant bioeroders. Like sponges, they bore mainly by chemically means, with some removal probably due to mechanical abrasion by saeta. Thereby, they are capable to reach erosion-rates of 1.8kg×m-2×a-1 (at population densities of 80×E3 individuals m-2). Most Cirratulid (like eunicid) species are predominantly deposit feeders whereas sabellids and spionids are mainly filter feeders.5.74

The most conspicuous tubicolous polychaetes are found among members of the families Serpulidae and Sabellidae; i.e. Spirobranchus giganteus; it's double whorls of branchiae resembles a small Christmas tree and may be found in all colors from black and white, to gray, blue, yellow, orange, or brilliant red. They occur mainly down the growing perimeter of micro-atolls formed by Porites lutea (fig.5.22). Interestingly, living Spirobranchus and rarely found in dead coral colonies.5.75 Some syllid species are known to eat live polyps, while others are found as ectoparasites on gorgonians. Equipped with a single large tooth and a powerful pharynx they graze polyps by simply sucking them out of their attachments.5.76a
Hermodice carunculata is a corallivorous polychaete and responsible for the destruction of living tissue of several hexacorals as well as the hydrocoral Millepora spp. on Caribbean reefs. With a removal rate of 0.13% per day it results in significant change in the relative abundance of this hydrozoan coral species.5.77 In the Mediterranean, H.carunculata has been found to harbour Vibrio shiloi in its gut (fig.5.23), thus acting as a reservoir to overcome the hostile winter season when hiding in the osculi of sponges.5.78 V.shiloi is a pathogen shown to induce bacterial bleaching in the Mediterranean coral O.patagonica (see VSB, Chapter-IV).5.79

Sipuncula:
Commonly also known as peanut worms, sipunculids occupy many niches within a coral reef ecosystem. Apart from boring geogenic substrate, some members are commonly found to bore into coral skeletons with others even gaining nutritive support from such an association. Yet still, there is no general agreement on the overall importance of these bioeroders. Because of low population densities no cases of coral mortality has been attributed to sipinculid activity so far. While Aspidosiphon elegans burrows into living corals, A.jukesi is found to live commensally in the base of the solitary coral Heteropsammia and Heterocyathus. Cleosiphon aspergillus and Lithacrosiphon cristatus on the other hand are common infauna of coral colonies.5.81a The exact manner of boring is not known, but may involve both chemical dissolution and mechanical abrasion.

 


Fig.5.22: Sessile polychaete (210kB) 5.76b
 

Fig.5.23: Mobile polychaete (140kB) 5.80
 

Fig.5.24: Sipunculid (70kB) 5.81b

Arthropoda:
Crustacea like barnacles, shrimp, hermit crabs, and others are also found to contribute in the erosion of reef rock. While barnacles and shrimp are endolithic borers, producing cylindrical chambers, hermit crabs are external bioeroders that abrade live coral surfaces.

Cirripedia: While most of the sessile barnacles of the order Thoracica (family Pyrgomatidae) are mere commensals, certain species such as Megatrema (Pyrgama) monticulariae, M.anglicum and Creusia spinulosa are true parasites of stony corals (fig.5.25). They not only depend on coral for food and habitat (feeding on the hosts soft tissue), but they actively interfere with the corals calcification process, tissue growth and nematocyst concentration. Their basal plate is attached at the innermost end of the cavity and the body hangs downward toward the opening with cirri exposed to food-bearing currents. The cavities are formed apparently by mechanical abrasion effected by calcified plates that cover the barnacle's body. Unlike other invertebrate endoliths, such as polychaete worms, and gastropods, adjacent tubes do interconnect; e.g. those of Lithotrya are commonly interwoven. Heavily infested substrates appear thoroughly honeycombed and are prone to frequent breakage. Lithotrya species erode 2-10cm long oval-shaped cavities on the undersides of reef rock and beach rock in shallow, agitated waters. Lithotrya sp. has also been found in corals, but damage is rather limited as they commonly reside in dead corals.5.82b

 


Fig.5.25: Cirripeds (175kB) 5.82c

Some members of the order Acrothoracica and Ascothoracica occupy small, millimeter-sized crevices, become embedded within the coral skeleton, and keep pace with the growth of the host coral without causing extensive erosion. Acrothoracica are also known as the burrowing barnacles and contrary to the thoracicans, possess a soft carapace (a-thoracic) with a reduced or absent calcareous plate (such as the brilliantly coloured Berndtia fossata).5.82a Members of Acrothoracica are fairly common parasites of deep-water gorgonians.
Stomatopoda: Mantis shrimp form a small group of highly successful predators that feed mainly on fish and molluscs. They live in a variety of habitats. Commonly encountered species such as Gonodactylus chiragra and G.smithii live in cavities of live or dead corals where the females guard the eggs.5.83

Decapoda: Although the majority of Alpheidae are free living, some even commensal on crinoids and sponges, and yet others live in remarkable association with gobies, considerable erosion can be caused by the pistol crabs Alpheus saxidomus, and A.simus which bore actively into coral rock (predominantly mechanically but also by chemical means). Due to the mechanical stress, the cheliped is subject to chronic abrasion. In such cases the bioerosive process comes to a halt until the animal regenerates the damaged right cheliped after molting is completed (ecdysis: shedding of the detached epidermis from the exoskeleton). Bioeroding decapoda can also be found among various other families, such as Crangonidae (Crangon sp.), the infraorders Brachyura and the families Thalassinidae and in particular those among Callianassidae such as Pomatogebia o. = Upogebia operculata). P.operculata live in pairs within the coral boulder to excavate tunnels. Both entrance and exit are sealed to leave just a tiny opening which enables them via their telsons to ventilate water through the system, and at the same time to filter-feed for suspended plankton. The few genera among the Cryptochiridae consists of obligatory associates of a variety of corals. In certain cases the relationship between the coral and the associated fauna is so specialized that some species are only found on particular corals. One such case is the gall crab Hapalocarcinus marsupialis found among Pocilloporidae (i.e. among Stylophora and Seriatopora colonies); its presence induces abnormal growth to the coral by developing a cage in which female individuals are entrapped only to be fertilized by the free-living males (compare fig. 5.25).5.84d Another interesting feature can be observed within the family Paguridae (fig.5.26); here Paguritta gracilepis and P.harmsi both prefer a sessile habitat and live within the skeleton of stony corals (particularly of Acropora species).5.84a

 


Fig.5.26: Decapods (180kB) 5.84b

Pantopoda: Pycnogonidae or sea spiders are small, almost transparent and parasitic to an unknown number of corals. They are most often reported in association with Acropora spp. and Pocillopora sp. corals, and will quickly remove tissue from infested corals. Their larvae may also pierce coral tissue, or parasitize them internally within the body wall or cavity of the polyp. Some young pycnogonids enter gorgonians through the polyp and remain encysted in them. SSpecies with predominantly parasitic and predatory characteristics can be found among the order Amphipods (sea fleas) and the morphologically very diverse order Isopoda, as well as within the class Ostracoda and the sublasses Copepoda. Some may form galls in coral tissue and may be true parasites, while others are merely commensal, living on coral mucus and associated flora and fauna. As such, they may perform a cleaning rather than a bioerosive function.5.85

Echinodermata:
Colourful echinoderms are among the most conspicuous reef invertebrates. While members in this phylum are harmless but highly mixotrophic, they consume what is available to them, thereby inadvertently become occasional coral grazers. Some notorious corallivorous seastars though, can be found in the class Stelleroidea: i.e. Culcita novaeguinae that among others feeds on juvenile Acropora and Pocillopora spp., and Acanthaster planci as the most significant coral predator. Members within the class Echinoidea (sea urchin) that feed on juvenile corals, include Diadema spp, while others may not just graze coral, but are real chasmoliths as they erode the surface to create a shallow depression in which they dwell.
Stelleroidea: Most asteroids are detritus feeders, some are omnivorous and only a few real predators like those two species Culcita and Acanthaster within the family Acanthasteridae (fig.5.27).
Acanthaster planci: This seastar of the tropical Indo-Pacific is unique in that it has a reduced skeleton and a pliable body form that allows access to a wide range of coral colony shapes. The normal densities of this starfish on Indo-Pacific reefs range from 6 to 20/km2, whereas outbreaks of A.planci result in numbers in excess of 500/km2.5.86 This seastar is a free-spawning, dioceious, sexually reproducing species, with females producing 12 to as many as 60E6 eggs per spawning season. Thus, even a few individuals grouped within short distance from each other can trigger a mass outbreak. In addition, outbreaks of A.planci have been correlated with storms on Pacific islands that deliver flushes of nutrient-rich runoff water to the coastal zone and in turn seem to enhance the survival and growth of starfish larvae.5.87
High population densities of A.planci are not sustainable, and community recovery of affected reefs occur over a time scale of 10-15 years, and only if no other disturbances do intervene with corals settlement, growth, or inter-specific competition with other benthic organisms.5.88

Culcita novaeguineae operates in similar manner. Because of its smaller extruded stomach area (compared to A.planci) it preys mainly on smaller colonies of acroporid and pocilloporid corals thus causing only minor effects on reef community structures.589 C.coriacea is another member of the above genus Culcita. Like other species of cushion stars it gains at least in part its nutrition from coral, but otherwise feeds on algae.590a


Fig.5.27: Corallivorous Asteroids (195kB) 590b

Echinoidea (sea urchins) are the only echinoderms (besides the seastar A.planci) capable of significant bioerosion. Several species abrade large amounts of reef rock while feeding and excavating burrows (e.g. species among the genera Diadema, Echinometra, Echinostrephus, and Eucidaris). Since urchins posses a highly evolved jaw apparatus (the Aristotle's lantern is a flexible and protrusible mastigatory organ consisting of five radially arranged, calcified teeth), they not only graze their way across the algal carpet (e.g. on dead corals), their spines also assist in bioerosion when they are employed in the enlargement of burrows.5.91

Diadema setosum, Echinothrix calamaris and Astropyga radiata are found in Zanzibar, while Diadema antillarum feeds on live stony corals and Echinometra lucunter being a true chasmolith. D.antillarum is a free-spawning echinoid with populations having a female-biased sex ratio of two to one. Spawning occurs year-round in small aggregations, with males and females at maximum within approx. 20cm spatial separation to achieve successful fertilization. Outbreak population densities of 3-73 ind/m2 are not uncommon (compare fig.5.28). D.antillarum inhabits holes and crevices diurnally, emerging at dusk to forage all night. While grazing by D.antillarum influences the survivorship and abundance of newly settled corals, the collapse of its population in 1983 to 2% of the outbreak population (probably the result of a viral pathogen) enabled macroalgae to colonize almost 95% of the substrate, thereby outcompeting coral recruits, triggering a shift from a coral dominated ecosystem to one dominated by algae (compare fig.3.3b and fig.3.7, Chapter-III).5.92 Although D.antillarum is an herbivore primarily feeding on algal turfs, endo- or chasmolithic cyanobacteria, and coralline algae (Porolithon, Neogoniolithon, Lithophyllum), it will prey also on live coral if nutritional limitations are encountered.5.93
Corallivorous Eucidaris species are often found to graze Pocillopora sp, while E.thouarsii feeds on a variety of encrusting animals as well as on crustose coralline algae causing in significant bioerosion of the coral framework in east-Pacific reefs of Panama and Ecuador.5.94a


 

Fig.5.28: Urchin-related Erosion (145kB) 5.94b

Fig.5.29: Echinoidea (145kB) 5.94c

Pencil urchins of the Indo-Pacific such as Heterocentrotus sp. bore into dead and occasionally live coral skeletons and rock (fig.5.29). Echinostrephus molaris instead is a true reef rock borer. Echinometra mathaei can be found in the same waters and likewise burrows extensively into the framework, thereby often responsible for the detachment of coral heads. It feeds on encrusting and upright algae in and near their protective crevices. The removal of echinoid predators (primarily via balistids and wrasses) easily leads to increases in population densities of E.mathaei by 2-3 orders of magnitude. As a result densities of E.mathaei reached 13 ind/m2 resulting in lowered algal biomass, increased bioerosion, and lowered spatial heterogeneity on heavily grazed reefs (along the coast of Kenya in 1989).5.95 As with the endolithic sponges spionid worms and lithophages, the bioerosive activity of Diadema, Echinometra, and Eucidaris can range from 3.5 to 22.3kg×m-2×a-1 (10-150 individuals/m-2). 5.96a
Thus the bioerosive properties, especially of echinoid species significantly determine the structural diversity of a reef. Thus, a slight change in population densities easily interferes with mechanical stability, and ultimately viability of massive and columnar coral colonies.

Ascidians:
The colonial species Lissoclinum patella (family Didemnidae) produces flattened masses with distinct valleys. The greenish colour is produced by the symbiotic cyanobacteria Prochloron. Hence, L.patella is often found in illuminated locations, thereby regularly competing with stony corals (fig.5.30). By secreting a toxic substance it retards coral growth (causing even necrosis and death) and thereby capable to gradually overgrow the coral from the bottom up.


Fig.5.30: Ascidians (140kB) 5.96b

Pisces:
Fish do significantly influence growth and condition of corals within a reef. Up to 68% of reef-fish species are carnivorous and erode coral substrata while grazing on algae and coral colony fragments. Thereby they feed on live coral tissues which enables them to extract invertebrates from coral colonies.5.97 Surgeonfishes (Acanthuridae) and parrotfishes (Scaridae) are the principal grazing groups with many fishes in the latter family capable of scraping and extensive excavation. Triggerfishes (Balistidae), filefishes (Monacanthidae), and puffers (Tetraodontidae) are largely carnivorous in feeding habits and are responsible for fragmenting live coral colonies. Based on the characteristic grazing pattern, coral preying fishes can be grouped into:

  • i) scrapers - Scaridae (Parrotfish like Sparisoma viride)
  • i) browsers - remaining Scaridae (other Parrotfish)
  • i) croppers - Tetraodontidae (Puffers, Arothron meleagris feeds predominantly on Pocillopora), Balistidae (Triggers)
  • i) suckers - Chaetodontidae (Butterfly)

Rapid Wasting Disease (RWD) is characterized by a rapid loss of tissue and destruction of the underlying coral skeleton; it is caused by parrotfish predation. Parrotfish inflict two distinct types of lesions ("spot-" and "focused-biting"). Spot biting in the western Atlantic is predominantly caused by roving schools of S.viride (fig.5.31). There, it is the only species that causes significant bioerosion and new sediment production. Bite marks are often paired, representing abrasions made by upper and lower dental plates, appearing as two elliptical scrapes separated by a narrow strip of unaffected tissue. Focused biting regards extensive removal of tissue and skeleton through repeated, overlapping bites by initial phase (IP) and terminal phase (TP) S.viride.

 


Fig.5.31: RWD (135kB) 5.98a

Parrotfish cause a great deal of bioerosion, due to their well developed jaw muscle and tooth armature, and a pharyngeal mill, which grinds up ingested material into sand-sized particles. M.annularis, M.faveolata and Colpophyllia natans are most frequently affected, but others of the g enera Acropora, Porites and Millepora are also grazed on. Tissue regenerates rapidly over spot bites, but remains pale and slightly depressed for several months. Usually, colonies affected by focused biting rarely experience total mortality. Observations in Puerto Rico however revealed that repeatedly preying groups of S.viride are able to kill entire colonies of C.natans.5.98b Surviving portions, typically the edges of the colony continue to grow upward and outward around a central depression that lacks tissue. Scarids have a particularly adapted pharyngeal mill which enables them to grind the material down to very fine silt (20m pellets). Defecation usually occurs in shallower water, while coral predation is most common at the reeffront. Being day active, they require feeding over 90% of their daytime in order to meet their metabolic requirements. As outlined with the erosion rates of endolithic sponges, spionid worms, lithophages, and echinoderms, parrotfish in particular are capable of relocating up to 1000kg×m-2×a-1 of carbonate substrate per individual (such as the Indo-Pacific Chlorurus gibbus with biting frequencies per individual ranging from 10 to 30/min). Thus, a slight change in population densities easily interferes with mechanical stability, and ultimately viability of massive and columnar coral colonies.5.99

Pomacentridae: Although most damselfish are omnivores and territorial species, the ones with the largest impact on corals are the Indo-Pacific herbivorous species regard Hemiglyphidodon plagiometopon and especially Stegastes lividus as well as S.nigricans (fig.5.32). In order to "cultivate" filamentous algae, the Caribbean Stegastes acapulcoensis repetitively nibble on coral polyps, thereby inducing localized coral necrosis, to ultimately establish algal mats that easily stretch over 0.25-0.5m2 per individual.5.99a They zealously defend their small algal plot against all intruders regardless of size (from the sea-urchins to the curios diver) yet still, adult Acanthurus triastegus (Acanthuridae) often take advantage of Pomacentrid cultivations and feed in large aggregations, thus overwhelming territorial damsels.5.99b


Fig.5.32: Pomacentridae (180kB) 5.99d

A healthy coral is capable to withstand the perpetually induced and localized necrosis. A weakened colony though may collapse altogether, especially if synergistic effects stress the coral from within and from outside. Coral death can also be induced when individual damsels group together in aggregations to establish their algal cultivation on a particular colony. The Caribbean damsel Eupomacentrus planifrons (= Stegastes planifrons) is capable to exert such stress momenta that Montastrea annularis and Acropora cervicornis often regress and die, whereas Dischistodus perspicillatus achieves similar results with Acropora palifera in the Pacific. On the other hand, such grazed spots deprived of an algal mat, are ideal settling substrates for new coral recruits.5.99c

Chaetodontidae: are among those corallivores that significantly alter scleractinian biota diversity - here in particular Chaetodon austriacus and C.trifascialis. Their preferences on particular coral species reduce growth rates and abundance of their primary coral species. C.trifascialis of the Red Sea, on the other hand predominantly feeds on Acropora valida, A.cytherea,, A.nasuta and A.humilis.5.99e C.trifasciatus predominantly feeds on polyps and mucus of Montipora- and Pocillopora-species, but has been observed to utilize Porites lobata and P.lutea as well. However, the massive survival of corallivores after the 1988 coral-bleaching event on Maldivian reefs suggests that some Chaetodontidae must have to some extend modified their corallivorous habits.5.99f

 


Fig.5.33: Chaetodon trifascialis (135kB) 5.99j

Acanthuridae aggregate to form smaller groups that graze over the reef. Ctenochaetus striatus for example is a typical browser, which utilizes horizontal, illuminated substrates5.99g and keeps dead portions of table-corals like A.clathrata and A.cytherea-group free from epilithic filamentous algae.5.99h Such browsers strip off the algal carpet, thereby facilitating recruitment by coral larvae. Acanthuridae and comparable species that graze, browse or plug algal mats across the reef system facilitate lateral enlargement of encrusting or massive coral species. It was documented that herbivorous Acanthuridae not only feed on epilithic algae but using their specialized jaws, they rasp off the uppermost layer of the calcareous substrate.5.99g Until recently, this kind of ichthyogenic bioerosion has only been associated to Scaridae.

 


Fig.5.34: Acanthurus triostegus (110kB) 5.99k

Excessive feeding pressure by these herbivorous species contributes to a net loss in reef accretion, however, they also keep weedy coral species like Acropora and Pocillopora at bay, thereby indirectly favouring development and proliferation of slow-growing and persistent coral species. Reefs damaged by bleaching revealed another interesting fact in that increased substrate availability was not compensated by increased herbivorous activity. Rather it was observed that filamentous algae gradually gave way to much more durable and less palatable algal species such as Derbesia. This shift is not only remarkable but works against a long-term recovery to a pre-bleached status in which scleractinian species dominate.5.99i

 

Please continue with Anthropogenic effects, Commercialization & Management of Coral Reefs - Chapter-VI