Previous Page Table of Contents Next Page


Parasites and biotic diseases in field and cultivated sea cucumbers

Igor Eeckhaut1,2, Eric Parmentier3, Pierre Becker1, Serge Gomez da Silva4 and Michel Jangoux1,2,4

1 Université de Mons-Hainaut, Mons, Belgium;2 Institut Halieutique et des Sciences Marines, Tulear, Madagascar; 3 Université de Liège, Liège, Belgium;4 Université Libre de Bruxelles, Bruxelles, Belgium

Abstract

Amongst echinoderms, the Holothuroidea represents the class that is the most infested by parasites. Parasites of holothuroids are bacteria, protozoa and metazoa. There are about 150 species of metazoans which parasite holothuroids. Most of them are turbellarians, gastropods, copepods, crabs or fishes. The main body sections suffering from infestations are the digestive system and the coelom. The diseases induced by metazoan parasites are mostly structural: they create galls at the surface of the epidermis, pierce the respiratory tree or dig into the body wall down to the coelom. Most metazoans that live in the digestive system do not induce obvious diseases and their relationship with their hosts is probably closer to commensalism. Most protozoa that parasite holothuroids are sporozoans. They occur mainly in the coelom and/or the haemal system, one species having been reported infesting the gonads. Even in heavily infested hosts, the signs of disease induced by sporozoans are low: at most, a host haemal lacuna is occluded by trophozoites, or cysts are formed in the coelomic epithelium.

The most pathogenic agents reported from cultured sea cucumbers are bacteria. Cultivated holothuroids may suffer from a bacterial disease, called skin ulceration disease that affects their body wall. In particular, juvenile Holothuria scabra reared in the Aqua-Lab hatchery of Toliara, Madagascar, suffered from such a disease that caused death within three days. The first sign of the infection is a white spot that appears on the integument of individuals, close to the cloacal aperture. The spot extends quickly onto the whole integument leading to the death of the specimen. The lesions consist of areas where the epidermis is totally destroyed and where collagen fibres and ossicles are exposed to the external medium. The area is surrounded by a border line where degrading epidermis is mixed with connective tissue. Three bacterial morphotypes have been identified: rod-shaped bacteria, rough ovoid bacteria and smooth ovoid bacteria. Furthermore, three species of bacteria have also been identified in the white spot lesions from biomolecular analyses (DGGE and sequencing): Vibrio sp., Bacteroides sp. and an a-proteobacterium.

Keywords: Parasitoses, bacteria, holothuroidea

Introduction

Many organisms are reported to infest echinoderms, especially holothuroids. Holothuroid associates are either commensals or parasites. The former are harmless to the hosts: they often live on the surface of holothuroids acting as protective coverings against predators. Parasites on the other hand are always harmful to their hosts and, although mainly non-lethal can cause the host’s death in some instances. For them, holothuroids provide biotic substrates where they can live, serving sometimes as a source of food and/or as a source of developmental stimuli without which they cannot complete their life cycle. According to a review on echinoderm diseases (Jangoux, 1990), more than one third of echinoderm parasites live in or on holothuroids. No bacteria had been recorded at that time and only protozoan and ten metazoan taxa of high rank in the Linnean hierarchy were known to infest holothuroids. According to Jangoux (1990), most parasitic animals were Platyhelminthes (39 turbellarian species and 3 flukes), followed by Mollusca (33 gastropods and 4 bivalves), Arthropoda (one tardigrade, 22 copepods, 8 crabs and 2 pycnogonids), Pisces (9 carapids), Bryozoa (4 species), Annelida (2 polychaetes) and finally Porifera, Cnidaria, Entoprocta (1 species each) and Nematoda (undetermined number of species).

The report covers the main parasites and biotic diseases of sea cucumbers and includes recent studies on the subject since the work of Jangoux (1990). It particularly emphasises new bacterial parasites and the diseases that they induce.

Bacteria

Almost nothing is known about bacterial parasites and diseases in holothuroids. Morgan (2000) reported that a broodstock of Holothuria scabra from Bribie Island (Australia) suffered from a bacterial disease. The infection provoked the loss of epidermal pigmentation associated with the presence of huge amounts of viscous mucus. The lesions first arose around the mouth and/or cloacal opening of the diseased animals and then spread on both sides of the individuals before possibly encompassing the whole body. If infected animals were not eliminated from the broodstock, up to 95 % of the reared individuals died (Morgan, 2000). According to this author, Vibrio harveyi was the predominant bacterium in the lesions of affected holothuroids.

Becker (2002) reported on a disease, called skin ulceration disease, affecting juvenile H. scabra reared in a hatchery at Toliara, Madagascar. Microscopic and biomolecular techniques (denaturing gradient gel electrophoresis and sequencing) together with bacterial cultures and infection assays were used to characterise the disease and to investigate the microbial communities of the lesions.

The skin ulceration disease, which affects the body wall of juvenile H. scabra at Toliara, appeared for the first time in September 2000 and broke out in February 2001, May 2001, February 2002 and July 2002. The infection extended very quickly in the aquaria, being highly contagious. In February 2001, the skin ulceration disease reached a peak and affected two thirds of the juveniles two days after its appearance. The disease was also highly virulent causing death three days after detection of the first symptoms.

The first obvious sign of the disease was the appearance of small, white, rounded spots of about 1 mm in diameter corresponding to areas where the epidermis was destroyed. The white colour of the lesions is due to exposure of the connective tissue that follows destruction of the cuticle, the epidermis and the upper part of the connective tissue.

Yet, the mesothelium, the muscles and the internal organs remained unaffected. The first white spots always appeared close to the cloacal opening and this was quickly followed by an outbreak of other spots similar in size, shape and colour in the posterior half of the individuals. The rest of the body remained healthy and the behaviour of diseased and healthy holothuroids was unchanged except that the former did not seem to burrow anymore. Twenty-four hours later, the white spots spread and joined together to form a large, posterior lesion which covered about a fifth of the body surface (Figure 1). Podia inside this lesion were totally destroyed. Other spots then appeared on the anterior part of the body and ossicles became visible externally, some of them separating from the integument. Forty-eight hours later, more than a half of the body surface was affected. Juveniles were much less active, became almost translucent, and their internal organs visible through the body wall. Three days after the beginning of the disease, the whole body surface was affected. Dead individuals were reduced to pellets of heavily infested tissue.

Figure 1. Juvenile of Holothuria scabra affected by the skin ulceration disease (O.M.). AZ: affected zone; CO: cloacal orifice; HZ: healthy zone. Scale bar = 100 mm.

With the use of scanning electron microscopy (SEM), two different zones of the body surface may be observed in the white spot lesions of diseased holothuroids: (1) the affected zone, colonised by microorganisms, where the epidermis and cuticle are totally destroyed and where a disorganised connective tissue is exposed to the medium and (2) a borderline of a few tens of micrometers wide where the surface is colonised by microorganisms and where patches of degrading epidermis are mixed with degrading, exposed connective tissue. In the affected zone, collagen fibres run in all directions, breaking off from each other while the ossicles, some of them highly degraded, are exposed to the external medium (Figure 2). Three bacterial morphotypes are observed in these two zones: rod-shaped bacteria, rough ovoid bacteria and smooth ovoid bacteria. The smooth ovoid bacteria were observed degrading holothuroid ossicles (Figure 3).

Figure 2. SEM views of a lesion of a Holothuria scabra juvenile affected by the skin ulceration disease showing degraded ossicles in the affected zone and smooth ovoid bacteria on an ossicle, respectively. Scale bars = 10 mm.

Figure 3. SEM views of a lesion of a Holothuria scabra juvenile affected by the skin ulceration disease showing smooth ovoid bacteria on a degrading ossicle. Scale bars = 5 mm.

The biomolecular techniques identified three species of bacteria in the lesions. The first, Vibrio sp., has been isolated in bacterial cultures of sea cucumber lesions and identified by DNA sequencing. The two other bacteria, Bacteroides sp. and an a-proteobacterium, have been detected by the denaturing gradient gel electrophoresis method.

From the three bacteria, Vibrio sp. is the best candidate as the etiological agent of the skin ulceration disease. It is indeed close to Vibrio harveyi and V. alginolyticus, two well-known pathogenic bacteria. Vibrio harveyi is responsible for numerous infections to both vertebrates and invertebrates.

Protozoa

Ciliates living in the digestive tract and in the respiratory trees of holothuroids have been reported by Barel and Kramer (1977). Holothuroids are otherwise mainly infested by members of five gregarine genera (13 described species) - Cystobia, Diplodina, Goniospora, Lithocystis and Urospora - and one species of coccidia (Ixoreis psychropotae). Deposit-feeding holothuroids are very sensitive to gregarine infestations. Kroll and Jangoux (1989), for example, observed that 90 % of the 50 Holothuria tubulosa collected in the Posidonia beds at Castello (Ischia Island, Italy) were infested by gregarines. The high infestations of holothuroids by gregarines can be explained by the fact that echinoderms may infest themselves simply by swallowing sediment that contains mature sporocysts. The life cycle of gregarines is complex and includes six developmental stages - sporocysts, sporozoites, trophozoites, gamontes, gametocysts and sporogonia - that are all observed within the holothuroids. Once in the digestive system, sporocysts are broken down and sporozoites are liberated owing to the physico-chemical properties of the digestive fluid (Jangoux, 1990). Generally, they penetrate cells of the digestive system and migrate into the haemal system or the coelom. A prolonged stay in the host’s haemal system is necessary for a few species, probably for most of them, but the described species are often known only from one stage that infested a specific host’s body part. Trophozoites and subsequent stages are extracellular and found in the haemal lacuna, attached to the coelomic epithelium or embedded in coelomic brown bodies. The escape of gregarines from the hosts is unknown though it is generally accepted that they leave holothuroids through evisceration or at the host’s death. Recently, Doignon et al. (2003) observed that the coelomic content (brown bodies and parasites) of Holothuria tubulosa is purged seasonally, a phenomenon that could exist in other species. To explain this coelomic purge, the main hypothesis was that it would be an indirect result of the host’s spawning as it occurs at that time: to discharge their gametes, holothuroids raise their body, adhere on the substratum by their posterior end and then contract muscles. This behaviour would cause an overpressure in the peri-cloacal end of the animal and consequently the expulsion of the coelomic fluids through the coelo-cloacal ducts, carrying the coelomic contents, brown bodies and parasites into the environment.

Diseases induced by protozoans to holothuroids are reduced to small internal wounds and no lethality due to gregarines has been described in the literature. Growth of the Cystobia trophozoites progressively occludes the host’s haemal lacuna and a particular haemal outgrowth is formed like a bell-clapper protruding into the coelomic cavity; the clapper represents the so-called “stalked gregarine” that is formed by an evagination of the underlying haemal lacuna whose distal end encloses an enlarged trophozoite or a cyst (Jangoux, 1990). One species, Diplodina gonadipertha, infests the gonads of Cucumaria frondosa and could partially destroy the gonads (Djakonov, 1923). The single species of Coccidia, Iroxeis psychropotae, lives in the gut-associated haemal system of deep sea holothuroids (Massin et al., 1978).

Metazoa

Platyhelminthes

Jangoux (1990) has found 5 Acoela, 34 Umagillidae (Rhabdocoela) and 3 Trematoda infesting holothuroids. Five umagillids have been described since his review (Table 1). The acoels are found mostly in the digestive tract of holothuroids, one species has been observed in the coelom and another one in the respiratory trees. Umagillids infest either the coelom or the digestive tract. Snyder (1980) could determine neither beneficial nor detrimental effects due to the occurrence of gut-associated umagillids. He concluded that these symbionts should be considered as commensals. In contrast, Shinn (1981) reported that the gut-associated umagillids always compete with their host for nutrients and thus may exert adverse effects. He noted that all the umagillids studied by him ingest intestinal host tissue and he considered that they parasite their hosts to varying degrees. Whether they are living in the gut or in the coelom, they breed in the hosts and release egg capsules. Egg capsules are defecated in gut-associated umagillids or are accumulated in the holothuroid body cavity in coelom-associated umagillids. Coelomic umagillids swim in the host’s body cavity and they are thought to ingest the host’s coelomic fluid together with coelomocytes (Shinn, 1983) or to feed on coelom-associated organisms such as ciliates (Jennings, 1980).

Table 1. New species of Platyhelminthes infesting holothuroids that have been described since the review by Jangoux (1990).

Turbellaria
Umagillidae

Host

Geographical area

Source

Anoplodium heronensis

Stichopus sp.

Great Barrier Reef, Australia

Canon (1990)

Anoplodium leighi

Stichopus sp.

New Zealand

Canon (1990)

Paranotothrix sp.

Various holothuroids

Seychelles

Martens and De Clerck (1994)

Anoplodium sp.

Stichopus variegatus
Actinopyga miliaris

Seychelles

Martens and De Clerck (1994)

Wahlia westbladi

Stichopus mollis

Australia

Jondelius (1996)

Infestations by umagillids can be very high. The 27 individuals of Thelenota anax, Holothuria fuscogilva, H. coluber and Actinopyga mauritiana collected in Hansa Bay (Papua New Guinea) were all infested by gut-associated umagillids and some of them by more than 200 flatworms (Eeckhaut, pers. obs.). Doignon et al. (2003) studied the infestation of H. tubulosa by the coelom-associated umagillid Anoplodium parasita. They observed that 26 holothuroids out of the 202 collected at Banyuls-sur-mer (France) were infested by one to six adult A. parasita. The infestation of the holothuroids by the turbellarian egg capsules was very important: 128 out of the 202 holothuroids inspected contained at least 6 and up to 10 000 egg capsules (mean of 1 433). Quite uniform throughout the year, the number of egg capsules found in the coelom as well as the number of holothuroids infested by egg capsules fall drastically in July. Interestingly, this period is the one where the gonads of holothuroids were fully developed. Doignon et al. (2003) suggested that the release of the egg capsules could occur through coelo-rectal ducts and would be an indirect result of the host spawning.

The flukes Himasthla leptosoma and Zoogonoides viviparus infest the body wall at the base of the buccal tentacles of Leptosynapta spp. The first species has also been observed in the brown bodies (Cuénot, 1892, 1912; Jangoux, 1990). A third species, Tetrarynchus holothuriae occurs in the body wall of Molpadia sp. (Shipley, 1903). Holothuroids are probably intermediate hosts for flukes. Sea birds are the definite hosts of Himasthla leptosoma.

Annelida

The most recent review on symbiotic polychaetes is the one of Martin and Britayev (1998). They have found 18 polychaete species commensal of holothuroids, and one parasite. The parasite, Ophryotrocha puerilis, occurs in the coelomic cavity of Ocnus planci from Napoli (Monticelli, 1892; Barel and Kramer, 1977; Jangoux, 1990). Ganapati and Rhadakrishna (1962) noted that 50 % of the holothuroids Molpadia sp. were infested by the small hesionid Ancistrocyllis sp. either in the digestive tract or respiratory trees. Commensal polychaetes are simply attached by their parapodia to the surface of holothuroids and are considered totally harmless to their hosts. Britayev and Lyskin (2002), however, recently demonstrated that Gastrolepia clavigera, the commonest Indo-Pacific polychaete associated to holothuroids, partially eats the host’s integument. Holothuroid spicules represented up to 75 % of the polychaete’s gut content. These results suggest that symbiotic polychaetes currently considered as commensals could be true parasites.

Mollusca

Four Bivalvia and 33 Gastropoda are known to infest holothuroids (Jangoux, 1990). Bivalves live in the cloaca or inhabit small pouches dug into the digestive wall of synaptid holothuroids (Jangoux, 1990). Gastropods are free on the body surface where they may induce galls, they are also found in the respiratory tree, the digestive tract or the coelom. Ectoparasitic gastropods feed on the host’s tissues or fluids using their proboscis, which penetrates deeply into the holothuroid body wall or crosses it to reach the coelomic cavity or the haemal system (Jangoux, 1990). Intradigestive symbionts enter the digestive tract in order to feed by puncturing the digestive wall (Jangoux, 1990). A special case of intradigestive symbiosis is the one developed by Megadenus cantharelloides which attaches to the digestive wall of Stichopus chloronotus with its proboscis reaching the host’s body wall in order to feed on dermal tissue (Humphreys and Lützen, 1972). With the exception of Gasterosiphon deimatis, which feed on haemal fluid (Koehler and Vaney, 1903), intracoelomic gastropods are believed to derive their energy from the host’s coelomic fluid by direct absorption of nutrients through their body wall (Jangoux, 1990).

Harmful effects of parasitic gastropods are not restricted to their feeding activities, but they may produce attachment lesions involving host reactions and induction of galls. It is also reported that the intracoelomic Entocolax spp. may castrate their hosts (Heding and Mandahl-Barth, 1938). So far, there is no data indicating that parasitic eulimids can seriously affect the holothuroid cycle and the ecological consequences of this parasitism may be quite limited for the holothuroid populations involved (Jangoux, 1990).

Arthropoda

Twelve pinnotherid crabs are associated with holothuroids. Most live in the respiratory trees or the posterior part of the digestive tract. One, Pinnotheres decanus, is rarely found in the coelomic cavity. Lissocarcinus orbicularis, the commonest Indo-Pacific crab associated with holothuroids, is often found walking on the host’s body surface. Presumably, holothuroid-associated crabs do not feed on host tissues and most of them do not cause any detrimental effects, except to slightly wound the wall of respiratory trees or cloaca (Jangoux, 1990). A notable exception to this rule is the pea crab, Pinnotheres halingi, which causes a significant atrophy of the right respiratory tree (Hamel et al., 1999).

At least eighty-five cases of association between holothuroids and copepods have been described to date. The symbiotic copepods belong to four classes (Harpacticoida, Cyclopoida, Poecilostomatoida and Siphonostomatoida) and the holothuroid hosts to more than twenty genera. But still, there is little information regarding the relations between hosts and symbionts (see, for example, Humes, 1980). Most associations reported essentially describe the localisation of the symbionts in regards to the host and the presence/absence of conspicuous characteristics that would be induced by the symbiont’s presence (Jangoux, 1990). In the majority of these associations (about 60 %), copepods are defined as external symbionts, with a rather unclear definition of their relations with the holothuroid host. Since the review by Jangoux (1990), only the work of Gomes da Silva (2001) focused on the biology of symbiotic copepods, i.e. the poecilostome Synaptiphilus luteus (Figure 4) and the siphonostome Allantogynus delamarei (Figure 5). The first has never been reported as free living and shows a wide range of host tolerance (weak specificity). Its hosts are the northern Atlantic synaptid holothuroids, Labidoplax digitata, Leptosynapta inhaerens, L. gallienei and L. bergensis (Bocquet, 1952; Bocquet and Stock, 1957; Humes, 1980). Gomes da Silva (2001) performed population studies on S. luteus and showed that, if females are encountered throughout the year on their hosts, infestation by males occurs seasonally, the males and females only being present simultaneously on the hosts for a restricted mating period. Gomes da Silva (2001) also studied the coelomocyte reaction induced by Allantogynus delamarei in the body cavity of the Mediterranean aspidochirotes holothuroids, H. tubulosa and H. poli. The parasite shows many peculiarities; no male is known, only the females and three larval stages are described (Changeux, 1958). The female shows a highly modified morphology. She secretes an incubating envelope in which she continuously secretes ovigerous sacs each containing two embryos. The female and her ovigerous sacs are embedded in this incubating envelope, from which only the buccal tube protrudes to puncture the mesothelium of the host’s coelomic cavity.

Figures 4 and 5. Ventral views of a female Synaptiphilus luteus and of a female Allantogynus delamarei, respectively. a1: antennula, a2: antenna, ade: distal endopodite article, m1: maxillula, m2: maxilla, mxp: maxillipede, o: laying orifice, l1 to l4: leg 1 to leg 4, l5: leg 5, r: caudal ramus, t: buccal tube.

Pisces

Although some pearlfish (Carapidae, Ophidiiformes) are free-living, this family includes fishes that are able to live in association with different invertebrates. The origin of “pearlfish” is the discovery of dead carapid fish, paralysed and completely covered by a nacreous substance in an oyster shell (Ballard, 1991). However, the majority of the species belonging to the Carapini tribe (Carapus spp. and Encheliophis spp.) are usually found in the respiratory trees or in the coelomic cavity of holothuroids or in the coelomic cavity of asteroids.

Pearlfishes associated with sea cucumbers are listed in Table 2. Although the fishes are able to enter different host species, they often show a preference to a specific one (Trott and Trott, 1972; Gustato et al., 1979). C. boraborensis, C. homei, C. mourlani and E. gracilis can live in the same host species and are found in the same waters, but they usually do not inhabit the same host individual (Smith, 1964; Trott, 1981; Shen and Yeh, 1987; Vandenspiegel and Jangoux, 1989; Markle and Olney, 1990). If it exists, a system of sea cucumber recognition is not yet correctly highlighted. These fish are able to produce sounds (Parmentier et al., 2003). It is believed that these sounds are not used by the fish to identify the presence of another fish in the holothuroid before penetration, but are produced in the presence of congeneric individuals, inside holothuroids (Parmentier et al., 2003). Pearlfish sound emissions could be a form of communication used where the visibility is strongly reduced and where chemical communications may be masked by the host.

Table 2. Fishes associated with echinoderms (Parmentier, 2003). (*) most common host (indicated when known); A: asteroid; B: bivalve; H: holothuroid.

Carapidae


Host

Author

Carapus acus

H

Stichopus regalis (*)

Arnold (1953, 1957), Gustato et al. (1979), Vitturi & Catalano

H

Holothuria tubulosa (*)

(1988), Kloss & Pfeiffer (2000) Arnold (1953, 1956, 1957),
Gustato et al. (1979), Vitturi &

H

Holothuria poli

Catalano (1988), Kloss & Pfeiffer (2000) Arnold (1956, 1957)

H

Holothuria helleri

Arnold (1956, 1957)

H

Holothuria sanctori

Arnold (1956)

Carapus bermudensis

H

Actinopyga agassizi (*)

Arnold (1956), Smith & Tyler (1969), Van Meter & Ache

H

Isiostichopus badionatus

(1974), Trott (1970), Smith et al. (1981), Tyler et al. (1992) Smith
and Tyler (1969)

H

Astichopus multifudus

Trott (1970)

H

Holothuria glaberrima

Trott (1970)

H

Holothuria princeps

Dawson (1971)

H

Holothuria lentiginosa

Miller & Pawson (1979), Valentine & Goeke (1983),

H

Holothuria mexicana

Smith & Tyler (1969), Trott (1970), Tyler et al. (1992)

Carapus mourlani

H

Culcita novaeguineae

Mortensen (1923), Petit (1934), Schultz (1960), Smith (1964), Trott (1970), Trott & Trott (1972), Meyer-Rochow (1977,

A

Pentaceros hawaiiensis

1979), Meyer-Rochow & Tiang (1978), Machida (1989)
Markle & Olney (1990)

A

Choriaster granulatus

Markle & Olney (1990)

A

Acanthaster planci

Cheney (1973), Machida (1989)

H

Stichopus variegatus

Markle & Olney (1990)

H

Stichopus chloronotus

Markle & Olney (1990)

H

Bohadschia argus

Trott (1970), Meyer-Rochow (1977), Machida (1989), Markle

H

Actinopyga mauritania

& Olney (1990) Markle & Olney (1990)

H

Holothuria scabra

Markle & Olney (1990)

Carapus homei

H

Bohadschia argus (*)

Smith (1964), Branch (1969), Trott (1970), VandenSpiegel &
Jangoux (1989), Markle & Olney (1990)

H

Stichopus chloronotus (*)

Smith (1964), Branch (1969), Trott (1970), Trott & Garth (1970),
Trott & Trott (1972), Seymour & McCosker (1974),

H

Stichopus variegatus

Markle & Olney (1990) Trott (1970), Meyer-Rochow (1977)

H

Thelenota ananas

Markle & Olney (1990)

H

Actinopyga echinites

Markle & Olney (1990)

H

Holothuria ocellata

VandenSpiegel & Jangoux (1989)

A

Culcita schmideliana

Hipeau-Jacquotte (1967), Jangoux (1974)

A

Mithrodia fisheri

Jangoux (1974)

B

Pteria lotorium

Mahadevan (1959)

Carapus boraborensis

H

Thelenota ananas

Smith (1964), Trott (1970), Meyer-Rochow (1977), Vanden
Spiegel & Jangoux (1989), Markle & Olney (1990)

H

Bohadschia argus

Smith (1964), Markle & Olney (1990), VandenSpiegel &

H

Stichopus chloronotus

Jangoux (1989) Markle & Olney (1990)

H

Pearsonothuria graeffei

VandenSpiegel & Jangoux (1989)

H

Thelenota anax

Ballard (1991) - Parmentier et al. (2002)

Encheliophis sagamianus

H

Holothuria mertensiothuria

Tanaka (1908), Arnold (1956)

A

Certonardoa semiregularis

Yosii (1928)

A

Nardoa semiregularis

Arnold (1956)

Encheliophis vermicularis

H

Holothuria kefersteinii

Trott (1970)

H

Holothuria leucospilota

Murdy & Cowan (1980), Masuda et al. (1984)

H

Holothuria lubrica

Steinbeck & Ricketts (1941)

H

Thelenota ananas

Markle & Olney (1990)

H

Holothuria atra

Schultz (1960)

H

Holothuria scabra

Murdy & Cowan (1980)

Encheliophis gracilis

H

Holothuria scabra

Arnold (1956)

H

Thelenota ananas

Shen & Yeh (1987), Markle & Olney (1990)

H

Holothuria atra

Strasburg (1961), Schultz (1960)

H

Actynopyga crassa

Markle & Olney (1990)

H

Bohadschia vitiensis

Markle & Olney (1990)

H

Bohadschia argus

Smith (1964), Trott (1970), Machida (1989), Markle & Olney

H

Stichopus chlroronotus

(1990) Smith (1964)

H

Holothuria chilensis

Trott (1970)

H

Stichopus sp.

Markle & Olney (1990)

A

Culcita discoidea

Arnold (1956)

A

Cuclcita novaeguineae)

Branch (1969), Trott (1970)

Encheliophis chardewalli

H

Actinopyga
mauritania

Parmentier (2003)

In most cases, there is only one fish per host. However, specimens of Encheliophis (E. gracilis, E. vermicularis and E. sagamianus) were reported to be sexually paired in various holothuroids (Murdy and Cowan, 1980; Trott, 1981). More than two specimens of C. homei, C. mourlani and C. bermudensis can be observed in the same host (Aronson and Mosher, 1951; Meyer-Rochow, 1977; Trott and Trott, 1972; Smith et al., 1981). Meyer-Rochow (1977) holds the record with fifteen C. mourlani in a specimen of Bohadschia argus. Although no data were reported in the literature, the presence of sexual pairs suggests that sea cucumbers serve also as breeding sites. Sea cucumbers also act as developmental stimulators for some carapid larvae. In Carapus and Encheliophis species, the penetration inside a sea cucumber is followed by heavy transformations during which the fish length is reduced by 60 %.

The stomach contents (Trott, 1970; Murdy and Cowan, 1980; VandenSpiegel and Jangoux, 1989) and the musculo-skeletal descriptions of the buccal and pharyngeal jaws (Parmentier et al., 1999, 2000a,b) have suggested different kinds of symbiosis depending on the species. Various authors have suggested that Carapus adults could be parasites (Arnold, 1953; Gustato, 1976; Trott, 1981), while others consider them as commensals, using their hosts as shelters and leaving them to hunt small preys such as annelids, crustaceans (shrimp, decapod, amphipod) and small fish (Trott, 1970; Meyer-Rochow, 1979; VandenSpiegel and Jangoux, 1989; Parmentier et al., 2000a,b). They can also be cannibals, feeding on other carapids within their host (Parmentier, pers. obs.). In contrast, Encheliophis species are true parasites, feeding on the internal tissues of their host, mainly the gonads (Smith, 1964; Trott, 1970; Trott and Trott, 1972; Murdy and Cowan, 1980; Trott, 1981).

Some individuals are frequently found in the general cavity of holothuroids, implying a perforation of the respiratory tree or the stomach. This kind of injury, also occurring when the fish leaves its host, should be negligible as pearlfish do not always infest the same host. However, in a heavily infested population, chances that a given host is regularly infested increase; hence, repeated loss of coelomic fluid and successive wound repairs have to be considered (Jangoux, 1990). On the other hand, Cuverian tubules are never exuded and holothuroid eviscerations do not seem to occur at the time of pearlfish entry.

General considerations

Platyhelminthes, Mollusca and Arthropoda are the taxa that include the highest numbers of holothuroid parasites but low attention has been devoted to holothuroid-associated gregarines and it is very probable that the number of infesting species recorded in the future will be higher than that of metazoan taxa (Figure 6). The digestive tract (including the cloaca) is the body part that is the most infested (Figure 7) and gut-associated parasites are flatworms, molluscs and crustaceans. Most of them are living free in the digestive tract, gliding on the digestive wall. The symbiotic relations that they develop with the holothuroids are still not well understood and their parasitic status relies more on suggestions than on true experiments. The coelom of holothuroids is also commonly infested and other flatworms, molluscs and crustaceans live there as well as protozoan gregarines and carapid fishes. Other body organs and systems, such as the haemal system, ambulacral system, respiratory trees, gonads and body wall are less affected by parasites. The body wall, in particular, is mainly affected by gastropods.

Figure 6. Number of species per taxon infesting holothuroids.

Infestation of holothuroids by internal parasites takes place mainly through body openings (mouth and cloacal aperture). Intracoelomic organisms reach the coelom by passing through the digestive wall. Intracoelomic copepods enter the coelom by penetrating the anterior part of the gut, larvae of most intracoelomic gastropods enter the coelom through the digestive wall and carapid fishes pierce the cloacal wall (Jangoux, 1990). Holothuroid reactions to parasites are of three types: (1) inflammatory-like reactions; (2) connective tissue reactions and (3) coelomocyte reaction (Jangoux, 1990). Inflammatory-like reactions consist of the migration of defensive cells (red spherules and coelomocytes) to the site of infection, and occur mainly with diseases caused by microorganisms. Connective tissue reactions counteract organisms such as gastropods that tend to stay within the connective tissue layer. Coelomocyte reactions are directed towards intracoelomic parasites and result in the phagocytosis or the walling off of foreign organisms.

Figure 7. Location of the parasites in the holothuroid body. When a parasite infested two body compartments, both have been included in the graph.

All the protozoans and metazoans parasites currently described in scientific literature are not lethal for wild or cultured adult holothuroids. They are thus of no economic importance and their presence in or on adult holothuroids should not alarm the sea cucumber industrial stockbreeders. However, it should be emphasised that high densities of holothuroid populations could favour overinfestation by parasites, and thus influence some important parameters in farming such as the growth rate of individuals or the reproductive abilities of breeders. Most alarming are the infections of sea cucumber juveniles by bacteria that can eradicate nearly all individuals of cultured populations in a few days. Parameters that cause the appearance of bacterial diseases are poorly known, but it is possible that an increase in temperature and/or too high density of individuals in aquaria can favour the infection of individuals. The best way to avoid such bacterial disease is to constantly check the health of juveniles and to remove sick individuals. Juveniles that are not too infected can recover by treating them with a faint formalin solution in salt water for a few minutes.

Acknowledgements

Thanks are expressed to Mr Alessandro Lovatelli for his kind invitation to the ASCAM workshop and to Dr J.-F. Hamel and Dr A. Mercier for having reviewed the manuscript. We are indebted to the Food and Agriculture Organization of the United Nations (FAO) for having financed the participation of Dr I. Eeckhaut at the ASCAM workshop. We also thank the Belgian Coopération Universitaire au Développement (CUD) and the Belgian National Fund for Scientific Research for their financial help during various field trips to Madagascar, without which this study would not have been possible. Acknowledgements are finally expressed to Man Wai Rabenevanana and Edouard Mara, Directors of the Institut Halieutique et des Sciences Marines (IHSM) of Toliara (Madagascar) and to all the people of this institution who contributed to the research project.

References

Arnold, D.C. 1953. Observation on Carapus acus (Brünnich) (Jugulares, Carapidae). Pubblicazioni della Stazione Zoologica di Napoli, 24:152-166.

Arnold, D.C. 1956. A systematic revision of the fishes of the teleost family Carapidae (Percomorphi, Blennioidea), with description of two new species. Bulletin of the British Museum (Natural History), 4:247-307.

Arnold, D.C. 1957. Further studies on the behaviour of the fish Carapus acus (Brünnich). Pubblicazioni della Stazione Zoologica di Napoli, 30:263-268.

Aronson, L.H. & Mosher, C. 1951. Observations on the behaviour and ecology of the West Indian pearlfish. Anatomical Record, 111:489.

Ballard, J. 1991. The pearlfish. African Wild, 45(1):16-19.

Barel, C.D. & Kramer, P.G. 1977. A survey of the echinoderm associates of the north-east Atlantic area. Zoologische Verhandelingen, Leiden, 156:1-159.

Becker, P. 2002. La maladie de la tache blanche chez l‘holothurie comestible commercialisée Holothuria scabra. Université de Mons-Hainaut. Master thesis. 55pp.

Bocquet, C. 1952. Copepods semi-parasites et parasites de la région de Roscoff. Description de Lichomolgus asterinae n.sp. Bulletin de la Société Zoologique de France, 77:495-504.

Bocquet, C. & Stock, J.H. 1957. Copépodes Parasites d’Invertébrés des Côtes de France, le genre Synaptiphilus Canu et Cuénot. Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen, Amsterdam, 60(5):680-695.

Branch, J.B. 1969. Observations on the ecology and behaviour of Guam pearlfishes (Carapidae). Micronesica, 24(2):274.

Britayev, T. & Lyskin, S. 2002. Feeding of the symbiotic polychaetes Gastrolepidia clavigera (Polynoidea) and its interactions with its hosts. Doklady Biological Sciences, 385:352-356.

Cannon, L.R.G. 1990. Anoplodium (Rhabdocoela, Platyhelminthes) endosymbionts of sea cucumbers from Australia and New Zealand. Zoologica Scripta, 19(4):395-402.

Changeux, J.P. 1958. Quelques caractèresbiologiques d’un copépodeparasite d’holothuries: Allantogynus delamarei n.g.n.sp. Comptes Rendus Hebdomadaire des Séances de l’Académie des Sciences, Paris 247:961-964.

Cheney, D.P. 1973. Pearlfish (Carapidae) in Acanthaster planci (L.). Micronesica, 9(1): 159.

Cuénot, L. 1892. Commensaux et parasites des échinodermes (deuxième note). Revue Biologique du Nord de la France, 5:1-22.

Cuénot, L. 1912. Contribution à la faune du Bassin d’Arcachon. V. Echinodermes. Bulletin de la Station biologique d’Arcachon, 14:17-116.

Dawson, C.E. 1971. Records on the pearlfish, Carapus bermudensis, in the northern Gulf of Mexico and of a new host species. Copeia, 1971:730-731.

Djakonov, M.D. 1923. Diplodina gonadipertha, n. sp. anew neogamus gregarine, parasite of the gonads of Cucumaria frondosa (Gunn.). Russkij Arkhiv Protistologie, 2:127-147.

Doignon, G., Jangoux, M., Féral, J.P. & Eeckhaut, I. 2003. Seasonal release of the egg capsules of Anoplodium parasita Shneider, 1858, intracoelomic turbellarian (Platyhelminthes, Rhabdocoel) symbiotic of the sea cucumber Holothuria tubulosa Gmelin, 1788 (Echinodermata, Holothuroidea). In: Echinoderm Research 2001. Féral J.P. and B. David (Eds.) p.261-264. Balkema, Rotterdam.

Ganapati, P.N. & Radhakrishna, Y. 1962. Inquilinism between a new hesionid polychaete and a holothurian Molpadia sp. Current Science, 31:382-383.

Gomes da Silva, S. 2001. Particularités de la biologie de deux coépodes symbiotiques d’holothuries: Synaptiphilus luteus Canu et Cuénot, 1892 et Allantogynus delamarei Changeux, 1958. Université Libre de Bruxelles. Master thesis. 56pp.

Gustato, G. 1976. Osservazioni sulla biologica e sul comportamento di Carapus acus (Ophioidei, Percomorphi). Bollettino Societá Naturalisti di Napoli, 85:505-535.

Gustato, G., Villari, A. & Villani, G. 1979. Ulteriori dati sul comportamento di Carapus acus (Gadiformes, Ophidiodei). Bollettino Societá Naturalisti di Napoli, 88:535-547.

Hamel, J.-F., Ng, P.K.L. & Mercier, A. 1999. Life cycle of the pea crab, Pinnotheres halingi, sp. nov., and obligate symbiont of the sea cucumber Holothuria scabra Jaeger. Ophelia, 50:149-175.

Heding, S.G. & Mandahl-Barth, G. 1938. Investigations on the anatomy and systematic position of the parasitic snail Entocolax. Voigtlaender Meddr Groenland, 108(5): 1-40.

Hipeau-Jacquotte, R. 1967. Notes de faunistique et biologie marines de Madagascar. IV. Observation sur le comportement du poisson Carapidae: Carapus homei (Richardson, 1844) de Madagascar. Recueils des Travaux de la Station Marine d’Endoume, 6:141-151.

Humes, A.G. 1980. A review of the copepods associated with holothurians, including new species from the Indo-Pacific. Beaufortia, 30(4):31-123.

Humphreys, W.F. & Lützen, J. 1972. Studies on parasitic gatsropods from echinoderms. II. On the structure and biology of the parasitic gastropod, Megadenus cantharelloides n. sp. Biologiske Skrifter, 19(1): 1-27.

Jangoux, M. 1974. Sur l’association entre certaines astéries (Echinodermata) et des poissons Carapidae. Revue Zoologique Afrique, 88:789-796.

Jangoux, M. 1990. Diseases of Echinodermata. In: Diseases of Marine Animals. Vol.3. Kinne, O. (Ed.). p.439-567. Biologische Anstalt Helgoland, Hamburg, Germany. 696 pp.

Jennings, J.B. 1980. Nutrition in Symbiotic Turbellaria. In: Nutrition in the Lower Metazoa. Smith D.C. and Y. Tiffon (Eds.). p.45-56. Pergamon Press, Oxford.

Jondelius, U. 1996. The echinoderm-inhabiting flatworms (Platyhelminthes, Rhabdocoela) from Western Australia. Belgian Journal of Zoology, 126(1):37-48.

Kloss, K. & Pfeiffer, W. 2000. Zur biologie des «eingeweidefisches» C. acus (Brunnich, 1768) (Carapidae, Teleostei), mit hinweisen auf eine nich-parasitische ernähung. Revue Suisse de Zoologie, 107(2):335-349.

Koehler, R. & Vaney, C. 1903. Entosiphon deimatis, nouveau mollusque parasite d’une holothurie abyssale. Revue Suisse de Zoologie, 11:23-41.

Kroll, A. & Jangoux, M. 1989. Les grégarines (Sporozoea) et les Umagillides (Turbellaria) parasites du coelome et du système hémal de l’holothurie Holothuria tubulosa Gmelin (Echinodermata). Vie marine, Marseille, 10:193-204.

Machida, Y. 1989. New distribution of the pearlfish, C. mourlani, with notes on its morphometry. Japanese Journal of Ichthyology, 36(3):363-368.

Mahadevan, S. 1959. On the occurrence of Fierasfer (Cuvier) homei as a commensal inside the bivalve Pteria lotorium Lamarck. Current Science, 3:129.

Markle, D.F. & Olney, J.E. 1990. Systematics of the Pearlfish (Pisces: Carapidae). Bulletin of Marine Science, 47(2):269-410.

Martens, E.E. & De Clerck, G.G. 1994. Interstitial and parasitic Platyhelminthes from the coast of the Seychelles. Oceanic reefs of the Seychelles, Netherlands Indian Ocean programme, Cruise reports, 2:97-106.

Martin, D. & Britayev, A. 1998. Symbiotic polychaetes: a review of known species. Oceanography and Marine Biology. An Annual Review, 36:217-340.

Massin, C., Jangoux, M. & Sibuet, M. 1978. Description d’Ixoreis psychropotae, nov. gen., nov. sp. coccidie parasite du tube digestif de l’holothurie abyssale Psychropotes longicauda. Théel Protistologica, 14:253-259.

Meyer-Rochow, V.B. 1977. Comparison between 15 Carapus mourlani in a single Holothurian and 19 carapus mourlani from starfish. Copeia, 1977(3):582-585.

Meyer-Rochow, V.B. 1979. Stomach and gut content of Carapus mourlani from starfish and a holothurian. Annales Zoologici Fennici, 16:287-289.

Meyer-Rochow, V.B. & Tiang, M.K. 1978. Visual behavior, eye and retina of the parasitic fish Carapus mourlani. Biological Bulletin, 155:576-585.

Miller, J.E. & Pawson, D.L. 1979. A new subspecies of Holothuria lentiginosa Marenzeller from the western Atlantic Ocean (Echinodermata: Holothuroidea). Proceedings of the Biological Society of Washington, 91:912-922.

Monticelli, F.S. 1892. Notizia preliminare intorno ad inquilini degli Holothuroidea del Golfo di Napoli. Monitore Zool. Ital., 3:249-256.

Morgan, A.D. 2000. Aspects de lagestion des stocks géniteurs d’holothuries de sable (Echinoderme: Holothurides). Secrétariat général de la Communauté duPacifique: La Beche-de-mer: Bulletin d’information, 13:2-8.

Mortensen, T. 1923. The Danish expedition to the Kei Islands 1922. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening, 76:55-100.

Murdy, E.O. & Cowan, M.E. 1980. Observation on the behaviour and symbiotic relationship of the pearlfish Encheliophis vermicularis (Osteichthys: Carapidae). Kalikasan. Philippine Journal of Biology, 9(2-3):309-312.

Parmentier, E. 2003. Contribution à l’étude des relations entre des poissons de la famille des Carapidae et leurs hôtes invertébrés: une approche multidisciplinaire. Université de Liège, PhD thesis. 229 pp.

Parmentier, E., Chardon, M., Poulicek, M., Bussers, J.C. & P. Vandewalle. 1999. Morphological particularities of the head in four Carapidae (Ophidiiformes). In: Proc. 5th Indo-Pacific Conf., Nouméa. 1997, Séret B and J.Y. Sire (Eds.). p. 135-146. Société Française Ichthyologique, Paris. 866pp.

Parmentier, E., Castillo, G., Chardon, M. & Vandewalle, P. 2000a. Phylogenetic analysis of the pearlfish tribe Carapini (Pisces: Carapidae). Acta Zoologica (Stockholm), 81:293-306.

Parmentier, E., Castro-Aguirre, J.L. & Vandewalle, P. 2000b. Morphological comparison of the buccal apparatus in two bivalve commensal Teleostei: Encheliophis dubius and Onuxodon fowleri (Carapidae, Ophidiiformes). Zoomorphology 2000, 120:29-37.

Parmentier, E., Vandewalle, P. & Lagardère, J.P. 2003. Sound producing mechanisms and recordings in three Carapidae species. Journal of Comparative Physiology, 189:283-292.

Petit, M.G. 1934. Un Fierasfer nouveau de Madagascar. Bulletin du Musée d’Histoire Naturelle de Paris, 2:393-397.

Schultz, L.P. 1960. Fishes of the Marshall and Marianas islands. Vol. II. Bulletin. United States National Museum, 202:1-418.

Seymour, R.S. & McCosker, J.E. 1974. Oxygen consumption of the commensal fish, Carapus homei. Copeia, 1974:971-972.

Shipley, A.E. 1903. On the ento-parasites collected by the “Skeat Expedition” to Lower Siam and Malay Peninsula in the years 1899-1900. Proceedings of the Zoological Society of London, 2:145-156.

Shen, S.C. & Yeh, H.S. 1987. Study on Pearlfishes (Ophidiiformes: Carapidae) of Taiwan. Journal of the Taiwan Museum, 40(2):45-56.

Shinn, G.L. 1981. The diet of three species of umagillid neorhabdocoel turbellarians inhabiting the intestine of echinoids. Hydrobiologia, 84:155-162.

Shinn, G.L. 1983. Anoplodium hymanae sp. n., an umagillid turbellarian from the coelom of Stichopus californicus, a northeast Pacific holothurian. Canadian Journal of Zoology, 61:750-760.

Smith, C.L. 1964. Some Pearlfishes from Guam, with notes on their ecology. Pacific Science, 18:34-40.

Smith, C.L. & Tyler, J.C. 1969. Observations on the commensal relationship of the western Atlantic pearlfish, Carapus bermudensis, and holothurians. Copeia, 1969:206-208.

Smith, C.L., Tyler, J.C. & Feinberg, M.N. 1981. Population ecology and biology of the pearlfish (Carapus bermudensis) in the lagoon at Bimini, Bahamas. Bulletin of Marine Science, 3:876-902.

Snyder, R.D. 1980. Commensal turbellarians from Bermuda holothurians. Canadian Journal of Zoology, 58:1741-1744.

Strasburg, D.W. 1961. Larval carapid fishes from Hawaii, with remarks on the ecology of adults. Copeia, 1961:478-480.

Tanaka, S. 1908. Description of eight new species of fishes from Japan. Annotationes Zoologicae Japoneses, 7:27-46.

Trott, L.B. 1970. Contribution of the biology of Carapid fishes (Paracanthopterygian: Gadiformes). University California Publications in Zoology, 89:1-41.

Trott, L.B. 1981. A general review of the pearlfishes (Pisces, Carapidae). Bulletin of Marine Science, 31(3):623-629.

Trott, L.B. & Garth, J.S. 1970. Lissocarcinus orbicularis Dana (Portunidae, Caphyrinidae), commensal with Holothuria argus Jaeger - A new host record; cohabitation with the pearlfish, Carapus homei (Richardson). Crustaceana, 19:30-321.

Trott, L.B. & Trott, E.B. 1972. Pearlfishes (Carapidae: Gadiforme) collected from Puerto Galera, Minobra, Philippines. Copeia, 1972:839-843.

Tyler, J.C., Robins, C.R., Smith, C.L. & Gilmore, R.G. 1992. Deepwater populations of the western atlantic pearlfish Carapus bermudensis (Ophidiiformes: Carapidae). Bulletin of Marine Science, 51(2):218-223.

Vanden Spiegel, D. & Jangoux, M. 1989. La symbiose entre poissons Carapidae et Holothuries autour de l’île de Laing (Mer de Bismarck, Papouasie Nouvelle Guinée). Indo-Malayan Zoology, 6:223-228.

Valentine, J.F. & Goeke, G.D. 1983. First record of Holothuria lentiginosa enodis Miller and Pawson (Echinodermata) in the northern Gulf of Mexico. Northeast Gulf Science, 6:155-156.

Van Meter V.B. & Ache, B.W. 1974. Host location by the pearlfish Carapus bermudensis. Marine Biology, 26:379-386.

Vitturi, R. & Catalanno, E. 1988. Karyotype of Carapus acus (Brünnich, 1768) (Pisces, Carapidae). Caryologia, 41:131-135.

Yosii, N. 1928. Note on a Carapus in a starfish. Annotationes Zoologicae Japoneses, 2:339-340.


Previous Page Top of Page Next Page