Adaptations of pearlfish (Carapidae) to their life inside sea cucumbers

[en] Carapidae (or pearlfish) are eel-like fishes that live inside different marine invertebrates, such as sea cucumbers, sea stars, and bivalves. Those in the genus Carapus are commensals and use their host as a shelter, while Encheliophis species are parasitic and eat the gonad(s) of their hosts. Life within the host requires different adaptations at the morphological and physiological levels. In this chapter, we have considered the different adaptations of symbiotic Carapus and Encheliophis species that have been investigated for living inside sea cucumbers and hope it can trigger new research in this field. Our discussion mainly focuses on the mode of penetration, diets, type of symbiotic relationships, morphological adaptations, breathing abilities, and resistance to host saponins in the fishes.

Research Center/Unit :

FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège

Disciplines :

Zoology

Author, co-author :

Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Language :

English

Title :

Adaptations of pearlfish (Carapidae) to their life inside sea cucumbers

Publication date :

November 2023

Main work title :

The World of Sea Cucumbers Challenges, Advances, and Innovations

Author, co-author :

Mercier Annie

Hamel Jean-François

Suhrbier Andrew

Pearce Christopher

Publisher :

Elsevier, Academic Press, London, United Kingdom

ISBN/EAN :

978-0-323-95377-1

Pages :

443-452

Peer reviewed :

Peer reviewed

Available on ORBi :

since 08 November 2023

Statistics

Number of views

23 (1 by ULiège)

Number of downloads

4 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenAlex citations

Bibliography

Anderson, M. E., & Satria, F. (2007). A new subfamily, genus, and species of pearlfish (Teleostei: Ophidiiformes: Carapidae) from deep water off Indonesia. Species Diversity, 12(2), 73-82.
Arnold, D. C. (1957). Further studies on the behaviour of the fish Carapus acus (Brunnich). 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.
Ayling, T., & Cox, G. J. (1982). Collins guide to the sea fishes of New Zealand. Williams Collins Publishers Ltd.
Bordbar, S., Anwar, F., & Saari, N. (2011). High-value components and bioactives from sea cucumbers for functional foods-a review. Marine Drugs, 9(10), 1761-1805. https://doi.org/10.3390/md9101761
Branch, J. B. (1969). Observations on the ecology and behaviour of Guam pearlfishes (Carapidae). Micronesica, 24, 274.
Brasseur, L., Parmentier, E., Caulier, G., Vanderplanck, M., Michez, D., Flammang, P., Gerbaux, P., Lognay, G., & Eeckhaut, I. (2016). Mechanisms involved in pearlfish resistance to holothuroid toxins. Marine Biology, 163(6). https://doi.org/10.1007/s00227-016-2901-3
Burnell, D. J., & Apsimon, J. W. (1983). Echinoderm saponins. Marine Natural Product in Chemistry and Biological Perpesctives, 5, 287-389.
Calabro, K., Kalahroodi, E. L., Rodrigues, D., Diaz, C., Cruz, M. de la, Cautain, B., Laville, R., Reyes, F., Perez, T., Soussi, B., & Thomas, O. P. (2017). Poecillastrosides, steroidal saponins from the Mediterranean deep-sea sponge Poecillastra compressa (Bowerbank, 1866). Marine Drugs, 15(7), 199. https://doi.org/10.3390/md15070199
Castro-Aguirre, J. L., Garcia-Dominguez, F., & Balart, E. F. (1996). Nuevos hospederos y datos morfometricos de Encheliophis dubius (Ophidiiformes : Carapidae) en el Golfo de California, Mexico). Revista de Biologia Tropical, 44, 753-756.
Caulier, G., Mezali, K., Soualili, D. L., Decroo, C., Demeyer, M., Eeckhaut, I., Gerbaux, P., & Flammang, P. (2016). Chemical characterization of saponins contained in the body wall and the Cuvierian tubules of the sea cucumber Holothuria (Platyperona) sanctori (Delle Chiaje, 1823). Biochemical Systematics and Ecology, 68, 119-127. https://doi.org/10.1016/j.bse.2016.06.005
Claereboudt, E. J. S., Caulier, G., Decroo, C., Colson, E., Gerbaux, P., Claereboudt, M. R., Schaller, H., Flammang, P., Deleu, M., & Eeckhaut, I. (2019). Triterpenoids in echinoderms: fundamental differences in diversity and biosynthetic pathways. Marine Drugs, 17, 352. https://doi.org/10.3390/md17060352
Claereboudt, E. J. S., Eeckhaut, I., Lins, L., & Deleu, M. (2018). How different sterols contribute to saponin tolerant plasma membranes in sea cucumbers. Scientific Reports, 8(1), 10845. https://doi.org/10.1038/s41598-018-29223-x
Codina, E., Loic, K., Compere, P., Dragicevic, B., Dulcic, J., & Parmentier, E. (2012). The barbel-like specialization of the pelvic fins in Ophidion rochei (Ophidiidae). Journal of Morphology, 273(12), 1367-1376. https://doi.org/10.1002/jmor.20066
Colleye, O., Brie, C., Malpot, E., Vandewalle, P., & Parmentier, E. (2008). Temporal variability of settlement in Carapidae larvae at Rangiroa atoll. Environmental Biology of Fishes, 81, 277-285. https://doi.org/10.1007/s10641-007-9199-4
Colleye, O., Kever, L., Lepoint, G., Lecchini, D., & Parmentier, E. (2018). Symbiotic relationship between the carapid fish Onuxodon fowleri (Ophidiiformes: Carapidae) and the pearl oyster Pinctada margaritifera (Mollusca: Bivalvia: Pteriidae). Scientia Marina, 82(1). https://doi.org/10.3989/scimar.04627.04A
Decroo, C., Colson, E., Demeyer, M., Lemaur, V., Caulier, G., Eeckhaut, I., Cornil, J., Flammang, P., & Gerbaux, P. (2017). Tackling saponin diversity in marine animals by mass spectrometry: data acquisition and integration. Analytical and Bioanalytical Chemistry, 409(12), 3115-3126. https://doi.org/10.1007/s00216-017-0252-7
Demeyer, M., Wisztorski, M., Decroo, C., De Winter, J., Caulier, G., Hennebert, E., Eeckhaut, I., Fournier, I., Flammang, P., & Gerbaux, P. (2015). Inter- and intra-organ spatial distributions of sea star saponins by MALDI imaging. Analytical and Bioanalytical Chemistry, 407(29), 8813-8824. https://doi.org/10.1007/s00216-015-9044-0
Eeckhaut, I., Caulier, G., Brasseur, L., Flammang, P., Gerbaux, P., & Parmentier, E. (2015). Effects of holothuroid ichtyotoxic saponins on the gills of free-living fishes and symbiotic pearlfishes. The Biological Bulletin, 228(3), 253-265. https://doi.org/10.1086/BBLv228n3p253
Emery, D. C. (1880). Fierasfer. Studi intorno alla sistematica, l’anatomia e la biologia delle specie mediterranee di questo di genere. Atti Accad Naz Lincei Cl Sci Fis Mat Nat Mem, 7, 167-316.
Enajjar, S., & Bradai, M. N. (2016). First Record of Carapus acus (Osteichthyes: Carapidae) in the Gulf of Gabes (southern Tunisia, central Mediterranean Sea). Marine Biodiversity Records, 9(1), 7. https://doi.org/10.1186/s41200-016-0015-8
Genta-Jouve, G., Boughanem, C., Ocana, O., Perez, T., Thomas, O. P., & Eryloside, W. (2015). A triterpenoid saponin from the sponge Dictyonella marsilii. Phytochemistry Letter, 13, 252-255.
Glynn, P. W., Enocbs, A. C., McCosker, J. E., & Graefe, A. N. (2008). First record of a pearlfish, Carapus mourlani, inhabiting the aplysiid opisthobranch mollusc Dolabella auricularia. Pacific Science, 62, 593-601. https://doi.org/10.2984/1534-6188(2008)62[593:FROAPC]2.0.CO;2
Govoni, J. J., Olney, J. E., Markle, D. F., & Curtsinger, W. R. (1984). Observations on structure and evaluation of possible functions of the vexillum in larval Carapidae (Ophidiiformes). Bulletin of Marine Science, 34, 60-70.
Govoni, J., Terwilliger, M., & Markle, D. (2015). Age, growth, and long-distance dispersal in the western North Atlantic of vexillifer larvae of the pearlfish, Echiodon dawsoni, with notes on Carapus bermudensis (Ophidiiformes: Carapidae). Ichthyological Research, 1-11. https://doi.org/10.1007/s10228-014-0455-2
Gustato, G. (1976). Osservazioni sulla biologica e sul comportamento di Carapus acus (Ophioidei, Percomorphi). Bollettino Della Societa Dei Naturalisti in Napoli, 85, 505-535.
Kever, L., Boyle, K. S., Bolen, G., Dragicevic, B., Dulcic, J., & Parmentier, E. (2014). Modifications in call characteristics and sonic apparatus morphology during puberty in Ophidion rochei (Actinopterygii: Ophidiidae). Journal of Morphology, 275, 650-660.
Kever, L., Colleye, O., Lugli, M., Lecchini, D., Lerouvreur, F., Herrel, A., & Parmentier, E. (2014). Sound production in Onuxodon fowleri (Carapidae) and its amplification by the host shell. Journal of Experimental Biology, 217, 4283-4294.
Kitagawa, I., & Kobayashi, M. (1977). On the structure of the major saponin from the starfish Acanthaster planci. Tetrahedron Letter, 18, 859-862.
Kloss, K., & Pfeiffer, W. (2000). Zur biologie des « eingeweidefisches » C. acus (Brunnich, 1768) (Carapidae, Teleostei), mit hinweisen auf eine nich-parasitische ernahung. Revue Suisse de Zoologie, 107, 335-349.
Kubanek, J., Pawlik, J. R., Eve, T. M., & Fenical, W. (2000). Triterpene glycosides defend the Caribbean reef sponge Erylus formosus from predatory fishes. Marine Ecology Progress Series, 207, 69-77. https://www.int-res.com/abstracts/meps/v207/p69-77/
Lagardere, J. P., Millot, S., & Parmentier, E. (2005). Aspects of sound communication in the pearlfish Carapus boraborensis and Carapus homei (Carapidae). Journal of Experimental Zoology Part A: Comparative Experimental Biology, 303(April), 1066-1074. https://doi.org/10.1002/jez.a.230
Li, R., Zhou, Y., Wu, Z., & Ding, L. (2006). ESI-QqTOF-MS/MS and APCI-IT-MS/MS analysis of steroid saponins from the rhizomes of Dioscorea panthaica. Journal of Mass Spectrometry, 41(1), 1-22. https://doi.org/https://doi.org/10.1002/jms.988
Mackie, A. M., & Turner, A. B. (1970). Partial characterization of a biologically active steroid glycosideisolated from the starfish Marthasterias glacialis. The Biochemical Journal, 117(3), 543-550. https://doi.org/10.1042/bj1170543
Markle, D. F., & Olney, J. E. (1990). Systematics of the pearlfishes (Pisces:Carapidae). Bulletin of Marine Science, 47(2), 269-410.
Matallanas, J., & Riba, G. (1980). Biological aspects of Ophidion barbatum Linnaeus, 1758 and O. rochei Muller, 1845 [sea snakes](Pisces, Ophidiidae) of the catalonian coast [Spain]. Investigacion Pesquera, Barcelona, 44, 399-406.
Meyer-Rochow, V. B. (1977). Comparison between 15 Carapus mourlani in a single Holoturian and 19 Carapus mourlani from starfish. Copeia, 1977, 582-585.
Meyer-Rochow, V. B. (1979). Stomach and gut content of Carapus mourlani from starfish and a holothurian. Annales of 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(3), 576-585. https://doi.org/10.2307/1540791
Millidine, K. J., Metcalfe, N. B., & Armstrong, J. D. (2008). The use of ventilation frequency as an accurate indicator of metabolic rate in juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences, 65(10), 2081-2087. https://doi.org/10.1139/F08-118
Mitu, S. A., Bose, U., Suwansa-ard, S., Turner, L. H., Zhao, M., Elizur, A., Ogbourne, S. M., Shaw, P. N., & Cummins, S. F. (2017). Evidence for a saponin biosynthesis pathway in the body wall of the commercially significant sea cucumber Holothuria scabra. In Marine Drugs, 15(11), 349. https://doi.org/10.3390/md15110349
Miyazaki, S., Ichiba, T., Reimer, J. D., & Junichi, T. (2014). Chemoattraction of the pearlfish Encheliophis vermicularis to the sea cucumber Holothuria leucospilota. Chemoecology, 24, 121-126. https://doi.org/DOI 10.1007/s00049-014-0152-7
Moss, M. L., & Murchison, E. (1966). Calcified anal teeth and pharyngeal ring in the holothurian, Actinopyga mauritania. Acta Anatomica, 64, 446-461.
Nielsen, J. G., Cohen, D. M., Markle, D. F., & Robins, C. R. (1999). FAO species catalogue. Ophidiiform fishes of the world (Order Ophidiiformes): An annotated and illustrated catalogue of pearlfishes, cusk-eels, brotulas and other ophidiiform fishes known to date. FAO Fisheries Synopsis No. 125, 18(125), 178.
Nigrelli, R. (1952). The effects of holothurin on fish, and mice with sarcoma 180. Zoologica, 37, 89-90.
Olney, J. E., & Markle, D. F. (1979). Description and occurrence of vexillifer larvae of Echiodon (Pisces : Carapidae) in the western North Atlantic and notes on other carapid vexillifers. Bulletin of Marine Science, 29, 365-379.
Padoa, E. (1947). Note di ittologia mediterranea. Nota V. Forme post-larvali egiovanili di Carapus (sin. Fierasfer). Pubblicazioni Della Stazione Zoologica Di Napoli, 20, 111-121.
Parmentier, E. (2004). Encheliophis chardewalli: a new species of Carapidae (Ophidiiformes) from French Polynesia, with a redescription of Encheliophis vermicularis. Copeia, 2004, 62-67.
Parmentier, E. (2016). Further insights into the metamorphosis process in a carapid fish. Journal of Zoology, 298(4), 249-256. https://doi.org/10.1111/jzo.12314
Parmentier, E., Bahri, M. A., Plenevaux, A., Fine, M. L., & Estrada, J. M. (2018). Sound production and sonic apparatus in deep-living cusk-eels (Genypterus chilensis and Genypterus maculatus). Deep Sea Research Part I: Oceanographic Research Papers, 141, 83-92. https://doi.org/https://doi.org/10.1016/j.dsr.2018.09.009
Parmentier, E., Castillo, G., Chardon, M., & Vandewalle, P. (2000). Phylogenetic analysis of thee pearlfish tribe Carapini (Pisces: Carapidae). Acta Zoologica, 81, 293-306.
Parmentier, E., Castro-Aguirre, J. L., & Vandewalle, P. (2000). Morphological comparison of the buccal apparatus in two bivalve commensal Teleostei, Encheliophis dubius and Onuxodon fowleri (Ophidiiformes, Carapidae). Zoomorphology, 120(592), 29-37. https://doi.org/10.1007/s004359900020
Parmentier, E., Chardon, M., Poulicek, M., Bussers, J. C., & Vandewalle, P. (1998). Morphology of the buccal apparatus and related structures in four species of Carapidae. Australian Journal of Zoology, 46, 391-404. https://doi.org/10.1071/ZO97035
Parmentier, E., Colleye, O., & Lecchini, D. (2016). New insights into sound production in Carapus mourlani (Carapidae). Bulletin of Marine Science, 92(3), 335-342. https://doi.org/10.5343/bms.2016.1014
Parmentier, E., & Das, K. (2004). Commensal vs. parasitic relationship between Carapini fish and their hosts: some further insight through δ13C and δ15N measurements. Journal of Experimental Marine Biology and Ecology, 310(1), 47-58. https://doi.org/https://doi.org/10.1016/j.jembe.2004.03.019
Parmentier, E., Fine, M. L., Berthe, C., & Lecchini, D. (2018). Taxonomic validation of Encheliophis chardewalli with description of calling abilities. Journal of Morphology, 279(7), 864-870. https://doi.org/10.1002/jmor.20816
Parmentier, E., Fine, M., Vandewalle, P., Ducamp, J. J., & Lagardere, J. P. (2006). Sound production in two carapids (Carapus acus and C. mourlani) and through the sea cucumber tegument. Acta Zoologica, 87(April), 113-119. https://doi.org/10.1111/j.1463-6395.2006.00221.x
Parmentier, E., Gennotte, V., Focant, B., Goffinet, G., & Vandewalle, P. (2003). Characterization of the primary sonic muscles in Carapus acus (Carapidae): a multidisciplinary approach. Proceedings of the Royal Society of London, Biological Science, 270(1530), 2301-2308. https://doi.org/10.1098/rspb.2003.2495
Parmentier, E., Lagardere, J. P., Chancerelle, Y., Dufrane, D., & Eeckhaut, I. (2008). Variations in sound-producing mechanism in the pearlfish Carapini (Carapidae). Journal of Zoology, 276, 266-275. https://doi.org/10.1111/j.1469-7998.2008.00486.x
Parmentier, E., Lanterbecq, D., & Eeckhaut, I. (2016). From commensalism to parasitism in Carapidae (Ophidiiformes): heterochronic modes of development? PeerJ, 4, e1786.
Parmentier, E., Lanterbecq, D., Todesco, M., & Eeckhaut, I. (2010). Unique morphologies of Encheliophis vermiops (Carapidae) with revised diagnosis of the genus. Ichthyological Research, 57, 85-90. https://doi.org/10.1007/s10228-009-0138-6
Parmentier, E., Lecchini, D., Lagardere, F., & Vandewalle, P. (2004). Ontogenic and ecological control of metamorphosis onset in a carapid fish, Carapus homei: experimental evidence from vertebra and otolith comparisons. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 301, 617-628. https://doi.org/10.1002/jez.a.50
Parmentier, E., Lecchini, D., & Vandewalle, P. (2004). Remodelling of the vertebral axis during metamorphic shrinkage in the pearlfish. Journal of Fish Biology, 64, 159-169. https://doi.org/10.1111/j.1095-8649.2004.00294.x
Parmentier, E., & Vandewalle, P. (2003). Morphological adaptations of Pearlfish (Carapidae) to their various Habitats. In A. L. Val & B. G. Kapoor (Eds.), Fish adaptations (pp. 261-276). Oxford & IBH.
Parmentier, E., & Vandewalle, P. (2005). Further insight on carapid-holothuroid relationships. Marine Biology, 146, 455-465. https://doi.org/10.1007/s00227-004-1467-7
Parmentier, E., Vandewalle, P., & Lagardere, J. P. (2003). Sound-producing mechanisms and recordings in Carapini species (Teleostei, Pisces). Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 189, 283-292. https://doi.org/10.1007/s00359-003-0401-7
Rogers, S. C., & Weatherley, A. H. (1983). The use of opercular muscle electromyograms as an indicator of the metabolic costs of fish activity in rainbow trout, Salmo gairdneri Richardson, as determined by radiotelemetry. Journal of Fish Biology, 23(5), 535-547. https://doi.org/https://doi.org/10.1111/j.1095-8649.1983.tb02933.x
Schwarz, C., Parmentier, E., Wiehr, S., & Gemballa, S. (2012). The locomotory system of pearlfish Carapus acus: what morphological features are characteristic for highly flexible fishes? Journal of Morphology, 273(5), 519-529. https://doi.org/10.1002/jmor.11038
Shen, S. ., & Yeh, H. S. (1987). Study on pearlfishes (Ophidiiformes: Carapidae) of Taiwan. Journal of the Taiwan Museum, 40, 45-56.
Smith, C. L. (1964). Some pearlfishes from Guam, with notes on their ecology. Pacific Science, 18, 34-40.
Smith, C. L., Tyler, J. C., & Feiberg, 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.
Trott, L. B. (1970). Contribution of the biology of carapid fishes (Paracanthopterygian: Gadiformes). University of California Publications in Zoology, 89, 1-41.
Trott, L. B. (1981). A general review of the pearlfishes (Pisces, Carapidae). Bulletin of Marine Science, 31, 623-629.
Trott, L. B., & Trott, E. B. (1972). Pearlfishes (Carapidae: Gadiforme) collected from Puerto Galera, Minobra, Philippines. Copeia, 1972, 829-843.
Tyler, J. C. (1970). A redescription of the inquiline carapid fish Onuxodon parvibrachium, with a discussion of the skull structure and the host. Bulletin of Marine Science, 20, 148-164.
Tyler, J. C., Robins, C. R., C.L., S., & Gilmore, R. G. (1992). Deepwater populations of the western atlantic pearlfish Carapus bermudensis (Ophidiiformes : Carapidae). Bulletin of Marine Science, 51, 218-223.
Van Den Spiegel, D., & Jangoux, M. (1989). La symbiose entre poissons Carapidae et Holoturies autour de l’ile de Laing (Mer de Bismarck, Papouasie Nouvelle Guinee). Indo-Mlayasan Zoology, 6, 223-228.
Van Dyck, S., Flammang, P., Meriaux, C., Bonnel, D., Salzet, M., Fournier, I., & Wisztorski, M. (2010). Localization of secondary metabolites in marine invertebrates: contribution of MALDI MSI for the study of saponins in cuvierian tubules of H. forskali. PLoS ONE, 5(11), e13923. https://doi.org/10.1371/journal.pone.0013923
Van Dyck, S., Gerbaux, P., & Flammang, P. (2009). Elucidation of molecular diversity and body distribution of saponins in the sea cucumber Holothuria forskali (Echinodermata) by mass spectrometry. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 152(2), 124-134. https://doi.org/https://doi.org/10.1016/j.cbpb.2008.10.011
Vandewalle, P., Parmentier, E., Poulicek, M., Bussers, J. C., & Chardon, M. (1998). Distinctive anatomical features of the branchial basket in four Carapidae species (Ophidiiformi, Paracanthopterygii). European Journal of Morphology, 36(3), 153-164.
Weber, M. (1913). Die Fische der Siboga-Expedition. Siboga-Expeditie, 32, 1-710.
Yamanouchi, T. (1955). On the poisonous substance contained in holothurians. Publications of the Seto Marine Biologyical Laboratory, 4, 183-203.