Skip to main content
Log in

The first record of symbiosis between a palaeonemertean (Nemertea) and echinoderms (Echinodermata)

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

The associations between Cephalotrichella echinicola Chernyshev et al., 2019, and the heart urchin Metallia spp. described here represent the first report on the symbiotic relationship between palaeonemerteans and echinoderms. In addition, it is the first report of a symbiotic relationship between nemerteans and heart urchins, and the third known association between nemerteans and echinoderms. Numerous specimens of C. echinicola were found associated with heart urchins Metallia spatagus and M. sternalis in four localities of the Bay of Nhatrang, Vietnam, South China Sea, at 6–10 m water depth buried in the coarse sand to a sediment depth of 10–20 cm. The infestation prevalence and mean intensity were higher in M. spatagus, than in M. sternalis, 77% and 68%, and 10 and 3 nemertean individuals per heart urchin host, respectively. Each infested host harbored from 1 to 49 nemertean individuals, and multiple infestations with three or more individuals per host were very common. Based on the high level of prevalence, absence of the nemertean on the other sand-dwelling heart urchins in the area, the complete absence of the nemerteans in the sandy bottom of the bay and in the sediment surrounded infested host individuals, and no reaction by the host to the nemertean’s movement on the host’s surface we consider this a symbiotic association.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baeza JA, Thiel M (2003) Predicting territorial behavior in symbiotic crabs using host characteristics: a comparative study and proposal of a model. Mar Biol 142:93–100

    Article  Google Scholar 

  • Barel CDN, Kramers PGN (1977) A survey of the echinoderm associates of the North-East Atlantic area. Zoologische Verhandelingen 156:11–59

    Google Scholar 

  • Britayev TA, Antokhina TI (2012) Symbiotic polychaetes from Nhatrang Bay, Vietnam. In: Britayev TA, Pavlov DS (eds) Benthic fauna of the bay of Nhatrang, Southern Vietnam, vol 2. KMK, Moscow, pp 11–54

    Google Scholar 

  • Britayev TA, Bratova OA, Dgebuadze PY (2013) Symbiotic assemblage associated with the tropical sea urchin, Salmacis bicolor (Echinoidea:Temnopleuridae) in the An Thoi Archipelago. Symbiosis 61:155–161

    Article  Google Scholar 

  • Bruce AJ (1982) The shrimps associated with Indo-West Pacific echinoderms, with the description of a new species in the genus Periclimenes Costa, 1844 (Crustacea: Pontoniinae). Mem Austr Mus 16:191–216

    Article  Google Scholar 

  • Castro P (2015) Symbiotic Brachyura. In: Castro P, Davie P, Guinot D, Schram FR, Vaupel Klein JC (eds) Decapoda: Brachyura, treatise on zoology – anatomy, taxonomy, biology, vol 9C-I. Brill, Leiden, pp 543–581

    Google Scholar 

  • Chernyshev AV (1991) Tetrastemma commensalis and Asteronemertes gibsoni gen. et sp. n. (Hoplonemertini, Tetrastemmidae) – commensals of starfish. Zoologicheskiy Zhurnal 70:34–39 (In Russian)

    Google Scholar 

  • Chernyshev AV (2016) Nemerteans of the coastal waters of Vietnam. In: Adrianov AV, Lutaenko KA (eds) Biodiversity of the Western Part of the South China Sea. Dalnauka, Vladivostok, pp 279–314

    Google Scholar 

  • Coe WR (1902) The nemertean parasites of crabs. Am Nat 36:431–450. https://doi.org/10.1086/278150

    Article  Google Scholar 

  • Dieck G (1874) Beiträge zur Entwicklungsgeschichte der Nemertinen. Jenaische Zeitschrift für Naturwissenschaft 8:500–520

    Google Scholar 

  • Egan EA (1984) The seasonal reproductive cycle of the nemertean Gononemertes australiensis Gibson in relation to that of its ascidian host, Pyura pachydermatina (Herdman). J Exp Mar Biol Ecol 76:225–246

    Article  Google Scholar 

  • Egan EA, Anderson DT (1979) The reproduction of the entozoic nemertean Gononemertes australiensis Gibson (Nemertea: Hoplonemertea: Monostylifera) - gonads, gametes, embryonic development and larval development. Aust J Mar Freshwat Res 30:661–681

    Article  Google Scholar 

  • Fleming LC, Gibson R (1981) A new genus and species of monostiliferous hoplonemerteans, ectohabitant on lobsters. J Exp Mar Biol Ecol 52:79–93

    Article  Google Scholar 

  • Gibson R (1967) Occurrence of the entocommensal rhynchocoelan, Malacobdella grossa, in the oval paddock, Zirfaea crispate, on the Yorkshire coast. J Mar Biol Assoc UK 47:301–317

    Article  Google Scholar 

  • Gibson R (1968) Studies on the biology of the entocornrnensal rhynchocoelan Malacobdella grossa. J Mar Biol Assoc UK 48:637–656

    Article  Google Scholar 

  • Gibson R (1974) A new species of commensal hoplonemertean from Australia. Zool J Linnean Soc 55:247–266

    Article  Google Scholar 

  • Gibson R (1986) Redescription and taxonomic reappraisal of Nemertopsis actinophilu Bürger, 1904 (Nemertea: Hoplonemertea: Monostilifera). Bull Mar Sci 39:42–60

    Google Scholar 

  • Gibson R, Sundberg P (1992) Three new nemerteans from Hong Kong. In: Morton B (ed) The marine flora and fauna of Hong Kong and southern China III, V. 1. University Press, Hong Kong, pp 97–129

    Google Scholar 

  • Hubrecht AAW (1879) The genera of European nemerteans critically revised, with description of several new species. Notes Leyden Mus 1:193–232

    Google Scholar 

  • Ivanov VA, Bigatti G, Penchaszadeh PE, Norenburg JL (2002) Malacobdella arrokeana (Nemertea: Bdellonemertea), a new species of nemertean from the southwestern Atlantic Ocean entocommensal in Panopea abbreviata (Bivalvia, Heterodonta, Hiatellidae) in Argentina. P Biol Soc Wash 115:359–367

    Google Scholar 

  • Jangoux M (1987a) Diseases of Echinodermata. II. Agents metazoans (Mesozoa to Biyozoa). Dis Aquat Org 2:205–234

    Article  Google Scholar 

  • Jangoux M (1987b) Diseases of Echinodermata. IV. Structural abnormalities and general considerations on biotic diseases. Dis Aquat Org 3:221–229

    Article  Google Scholar 

  • Kozloff EN (1991) Malacobdella siliquae sp. nov. and Malacobdella macomae sp.nov., commensal nemerteans from bivalve mollusks on the Pacific coast of North America. Can J Zool 66:1612–1618

    Article  Google Scholar 

  • Kuris AM (1993) Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories. Hydrobiologia 266:1–14

    Article  Google Scholar 

  • Kyao NI (1954) A new species of nemerteans, Amphiporus commensalis sp. n., from ambulacral grooves of the starfish Crossaster papposus. Uchenye zapiski Leningradskogo Universiteta. Seriya Biologicheskikh Nauk 35:135–139 (In Russian)

    Google Scholar 

  • Maran BAV, Kim I-H, Bratova OA, Ivanenko VN (2017) Two new species of poecilostomatoid copepods symbiotic on the venomous echinoid Toxopneustes pileolus (Lamarck) (Echinodermata) from Vietnam. Syst Parasitol 94:227–241

    Article  Google Scholar 

  • Martin D, Britayev TA (1998) Symbiotic polychaetes: review of known species. Oceanogr Mar Biol Annu Rev 36:217–340

    Google Scholar 

  • McDermott JJ, Gibson R (1993) Carcinonemertes pinnotheridophila sp. nov. (Nemertea, Enopla, Carcinonemertidae) from the branchial chambers of Pinnixa chaetopterana (Crustacea, Decapoda, Pinnotheridae): description, incidence and biological relationships with the host. Hydrobiologia 266:57–80

    Article  Google Scholar 

  • Odum EP (1971) Fundamentals of Ecology, 3d edn. WB Saunders Co., Philadelphia

  • Santos C, Norenburg JL, Bueno SL (2006) Three new species of Carcinonemertes (Nemertea, Carcinonemertidae) from the southeastern coast of Brazil. J Nat Hist 40(15–16):915–930

    Article  Google Scholar 

  • Senz W (2000) Neue Nemertinen aus dem Golf von Arabien. 1. Palaeonemertini. Ann Naturhist Mus Wien, Ser B Bot Zool 102B:321–373

  • Storch V, Niggemann R (1967) Auf Echinodermen lebende Polychaeten. Kiel Meeresforsch 23:156–164

    Google Scholar 

  • Thiel M, Francés-Zubillaga G (1998) Temporal and spatial occurrence of Tetrastemma fozensis in intertidal bivalves. Hydrobiologia 265:257–262

    Google Scholar 

  • Thiel M, Kruse I (2001) Status of the Nemertea as predators in marine ecosystems. Hydrobiologia 456:21–32

    Article  Google Scholar 

  • Udalov A, Britayev T, Than TH (2006) Features of the soft-bottom subtidal macrobenthos in Nha Trang Bay (Vietnam, South China Sea). Oceanology 46(4):483–491. https://doi.org/10.1134/S0001437006040059

    Article  Google Scholar 

  • Wickham DE, Kuris AM (1988) Diversity among nemertean egg predators of decapod crustaceans. Hydrobiologia 156:23–30. https://doi.org/10.1007/BF00027974

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Inc., Englewood Cliffs

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the administration of Coastal Branch of the Russian-Vietnam Tropical Center for their help in organizing and conducting field studies, and approval the collection of the samples and animals used in our article, our colleagues Mrs. Hai Thanh Nguyen, Mr. Tchan Than Kuang, Mr. N.L. Filichev, Dr. P. Dgebuadze, O. Savinkin, Yu. Deart for their help and collaborative work in the field.

Funding

Material processing and preparation of the manuscript were supported by the Russian Foundation for Basic Research; project no. 18–05-00459.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Temir A. Britayev.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for animal testing, animal care and use of animals were followed by the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Britayev, T.A., Bratova, O., Mekhova, E.S. et al. The first record of symbiosis between a palaeonemertean (Nemertea) and echinoderms (Echinodermata). Symbiosis 78, 135–139 (2019). https://doi.org/10.1007/s13199-018-00588-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-018-00588-x

Keywords

Navigation