Abstract
Myzostoma khanhkhoaense is a cyst-to-free-moving myzostomid associated with the comatulid crinoid Clarkcomanthus albinotus. It induces deformations of the skeletal elements of the host’s arms, thereby making protective “baskets” in which to hide from predators. Each “basket” is inhabited by a dense aggregation up to 25 worms of different sizes. The size-abundance structure of some subpopulations (these being defined as the inhabitants of one host) shows a clear peak, which may be related to the worm’s reproductive cycle. Some subpopulations show two such peaks, which may be evidence of colonization by two different generations of worms. No subpopulations with more than two peaks were found, what is probably an indication that these worms have a short lifetime. We believe that a newly settled generation of M. khanhkhoaense undergoes no more than two reproductive cycles, starting with initial settlement, growth, and reproduction, and then — evident as the larger-size peak if a second generation of larvae settles on the same host — another round of growth and reproduction, and finally death.
Similar content being viewed by others
Data availability
All material is available on request.
Code availability
Not applicable.
References
Atkins D (1927) Report on the Myzostomida collected by Mr. F.A. Potts in Torres Strait, together with a description of a species obtained by Professor J. Stanley Gardiner from the Maldives. Proc Zool Soc Lond 27:339–357
Baumiller TK, Gahn FJ (2013) Reconstructing predation pressure on crinoids: estimating arm-loss rates from regenerating arms. Paleobiol 39(1):40–51
Baumiller TK, Stevenson A (2018) Reconstructing predation intensity on crinoids using longitudinal and cross-sectional approaches. Swiss J Palaeontol 137:189–196. https://doi.org/10.1007/s13358-018-0169-6
Beard J (1884) On the life-history and development of the genus Myzostoma (F. S. Leuckhart). Mitt Zool Stat Neapel 5(3/4):544–580
Beesley PL, Ross GJB, Glasby CL (2000) Polychaetes and allies: the southern synthesis. Fauna of Australia, A Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. CSIRO Publishing, Melbourne
Bleidorn C, Eeckhaut I, Podsiadlowski L, Schult N, McHugh D, Halanych KM, Milinkovitch MC, Tiedemann R (2007) Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation. Mol Biol Evol 24(8):1690–1701. https://doi.org/10.1093/molbev/msm086
Britayev TA, Mekhova ES (2011) Assessment of hidden diversity of crinoids and their symbionts in the Bay of Nhatrang, Vietnam. Org Divers Evol 11(4):275–285. https://doi.org/10.1007/s13127-011-0053-3
Byrne M, Fontaine AR (1981) The feeding behaviour of Florometra serratissima (Echinodermata: Crinoidea). Can J Zool 59(1):11–18
Deheyn DD, Lyskin S, Eeckhaut I (2006) Assemblages of symbionts in tropical shallow-water crinoids and assessment of symbionts’ host-specificity. Symbiosis 42:161–168
Eeckhaut I, Grygier MJ, Deheyn D (1998) Myzostomids from Papua New Guinea, with related Indo-West Pacific distribution records and description of five new species. Bull Mar Sci 62:841–886
Eeckhaut I, Jangoux M (1993) Integument and epidermal sensory structures of Myzostoma cirriferum (Myzostomida). Zoomorphology 113(1):33–45
Eeckhaut I, Jangoux M (1997) Infestation, population dynamics, growth and reproductive cycle of Myzostoma cirriferum (Myzostomida), an obligate symbiont of the comatulid crinoid Antedon bifida (Crinoidea, Echinodermata). Cah Biol Mar 38(1):7–18
Eeckhaut I, Lanterbecq D (2005) Myzostomida: a review of the phylogeny and ultrastructure. Hydrobiologia 535/536:253–275. https://doi.org/10.1007/s10750-004-5636-y
Eeckhaut I, Lanterbecq D (2019) Myzostomida. In: Purschke G, Böggemann M, Westheide W (eds) Handbook of Zoology, vol 3. Pleistoannnelida, Sedentaria III and Errantia I. De Gruyter, Berlin, pp 1–36
Eeckhaut I, Dochy B, Jangoux M (1995) Functional morphology of the introvert and digestive system of Myzostoma cirriferum (Myzostomida). Acta Zool (Stockh) 76(4):307–315
Eeckhaut I, McHugh D, Mardulyn P, Tiedemann R, Monteyne D, Jangoux M, Milinkovitch MC (2000) Myzostomida: a link between trochozoans and flatworms? Proc R Soc Lond 267:1383–1392. https://doi.org/10.1098/rspb.2000.1154
Eeckhaut I, Fievez L, Müller CMM (2003) Larval development of Myzostoma cirriferum (Myzostomida). J Morphol 258(3):269–283. https://doi.org/10.1002/jmor.10160
Fabricius KE, Dale MB (1993) Multispecies associations of symbionts on shallow water crinoids of the central Great Barrier Reef. Coenoses 8(1):41–52
Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Ann Rev 17:193–284
Fedotov DM (1925) Über eine neue Art von Protomyzostomum (Pr. astrocladi, sp. n.) aus Astrocladus. Zool Anz 73:183–194
Fishelson L (1974) Ecology of the northern Red Sea crinoids and their epi-and endozoic fauna. Mar Biol 26(2):183–192
Gopko M, Mikheev VN (2017) Parasitic manipulations of the host phenotype: Effects in the internal and external environments. Zh Obshch Biol 78(6):16–48 [In Russian]
Grygier MJ (2000) Class Myzostomida. In: Beesley P, Ross GJB, Glasby CJ (eds) Polychaetes and allies: the southern synthesis. Fauna of Australia, vol. 4A. CSIRO Publishing, Melbourne, pp 297–329
Helm C, Weigert A, Mayer G, Bleidorn C (2013) Myoanatomy of Myzostoma cirriferum (Annelida, Myzostomida): implications for the evolution of the myzostomid body plan. J Morphol 274:456–466. https://doi.org/10.1002/jmor.20107
Huang HD, Rittschof D, Jeng MS (2005) Multispecies associations of macrosymbionts on the comatulid crinoid Comanthina schlegeli (Carpenter) in southern Taiwan. Symbiosis 39:47–51
Jägersten G (1939) Zur Kenntnis der Morphologie, Entwicklung und Taxonomie der Myzostomida. Nova Acta Reg Soc Sci Upsal Series 4 11(8):1–84
Jangoux M (1987) Diseases of Echinodermata. III. Agents metazoans (Annelida to Pisces). Dis Aquat Org 3:59–83
Kasumyan A, Isaeva O, Dgebuadze P, Mekhova E, Oanh LTK, Britayev T (2020) Comatulids (Crinoidea, Comatulida) chemically defend against coral fish by themselves, without assistance from their symbionts. Sci Rep 10:6150. https://doi.org/10.1038/s41598-020-63140-2
Kolbasova GD, Mekhova ES (2019) Myzostoma khanhkhoaensis (Myzostomida), a new myzostomid species from the Nhatrang Bay, Vietnam. Zootaxa 4691(3):235–249. https://doi.org/10.11646/zootaxa.4691.3.4
Kranz J (1993) Introduction to sampling in crop protection. In: Kranz J, Holz F (eds) Basics of decision-making and planning for integrated pest management (IPM). Federal Republic of Germany, Deutsche Stiftung für Internationale Entwicklung (DSE) und Zentralstelle für Ernährung und Landwirtschaft (ZEL), Feldafing, pp 33–45
Lanterbecq D, Eeckhaut I (2003) Myzostomida from Madagascar, with the description of two new species. Hydrobiologia 496:115–123. https://doi.org/10.1023/A:1026180428299
Lanterbecq D, Rouse GW, Milinkovitch MC, Eeckhaut I (2006) Molecular phylogenetic analyses indicate multiple independent emergences of parasitism in Myzostomida (Protostomia). Syst Biol 55(2):208–227. https://doi.org/10.1080/10635150500481317
Lanterbecq D, Hempson T, Griffiths C, Eeckhaut I (2009) Myzostoma fuscomaculatum (Myzostomida), a new myzostome species from False Bay, South Africa. Hydrobiologia 619(1):145–154. https://doi.org/10.1007/s10750-008-9606-7
Lanterbecq D, Rouse GW, Eeckhaut I (2010) Evidence for cospeciation events in the host–symbiont system involving crinoids (Echinodermata) and their obligate associates, the myzostomids (Myzostomida, Annelida). Mol Phyl Evol 54(2):357–371. https://doi.org/10.1016/j.ympev.2009.08.011
Leuckart FS (1836) In Beziehung auf den Haarstern (Comatula) und Pentacrinus europaeus, so wie auf das Schmarotzerthier auf Comatula. Notizen aus dem Gebiete der Natur- und Heilkunde 1087:129–131
Macurda DB, Meyer DL (1974) Feeding posture of modern stalked crinoids. Nature 247(5440):394–396
Macurda DB, Meyer DL (1983) Sea lilies and feather stars. Am Sci 71(4):354–365
Mecznikov E (1866) Zur Entwicklungsgeschichte von Myzostomum. Z Wiss Zool 16:236–244
Müller MC, Westheide W (2000) Structure of the nervous system of Myzostoma cirriferum (Annelida) as revealed by immunohistochemistry and cLSM analyses. J Morphol 245(2):87–98. https://doi.org/10.1002/1097-4687(200008)245:2%3c87::AID-JMOR1%3e3.0.CO;2-W
Nansen F (1885) Bidrag til Myzostomernes Anatomi og Histologi. John Griegs Bogtrykkeri, Bergen
Odum EP, Barrett GW (1971) Fundamentals of ecology. Saunders, Philadelphia
Rowe FWE, Hoggett AK, Birtles RA, Vail LL (1986) Revision of some comasterid genera from Australia (Echinodermata: Crinoidea), with descriptions of two new genera and nine new species. J Linn Soc (Zool) 86(3):197–277
Summers MM, Rouse GW (2014) Phylogeny of Myzostomida (Annelida) and their relationships with echinoderm hosts. BMC Evol Biol 14:170. https://doi.org/10.1186/s12862-014-0170-7
Summers MM, Al-Hakim II, Rouse GW (2014) Turbo-taxonomy: 21 new species of Myzostomida (Annelida). Zootaxa 3873(4):301–344. https://doi.org/10.11646/zootaxa.3873.4.1
Terrana L, Eeckhaut I (2017) Taxonomic description and 3D modelling of a new species of myzostomid (Annelida, Myzostomida) associated with black corals from Madagascar. Zootaxa 4244(2):277–295. https://doi.org/10.11646/zootaxa.4244.2.9
von Graff L (1877) Das Genus Myzostoma (F.S. Leuckhart). Wilhelm Engelmann, Leipzig
von Graff L (1887) Report on the Myzostomida collected during the Voyage of H.M.S. Challenger during the years 1873–76. Supplement. Report on the Scientific Results of the Voyage of H.M.S. Challenger during the Years 1873–76. Zoology 20:1–16
von Stummer-Traunfels RR (1903) Beiträge zur Anatomie und Histologie der Myzostomen. I. Myzostoma asteriae Marenz. Zeitschr Wiss Zool 85:495–595
Wagner FV (1886) Myzostoma bucchichii (nova species). Zool Anz 10:363–364
Wheeler WM (1896) The sexual phases of Myzostoma. Mitth Zool Stat Neapel 12:227–302
Woodham A (1992) Distribution and population studies on Myzostoma cirriferum Leuckart (Myzostomida) in a Scottish sea loch. In: Colombo G (ed) Marine Eutrophication and Population Dynamics: 25th European Marine Biology Symposium, Institute of Zoology, University of Ferrara International symposium series. Olsen & Olsen, Fredensborg, pp 247–255
Zar JH (1984) “Simple” linear regression. Biostat Analysis 4:324–359
Zrzavý J, Hypša V, Tietz DF (2001) Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella. Cladistics 17(2):170–198. https://doi.org/10.1006/clad.2000.0148
Acknowledgements
We would like to thank Drs. Temir Britayev and Alexander Tzetlin for valuable remarks on earlier drafts of this paper. We are also grateful to employees of the Joint Russian-Vietnamese Tropical Scientific and Technological Centre for their cooperation and assistance. Finally, our thanks are extended to Mr. Anatoly Bogdanov and Mr. George Davidovich (Laboratory of Electron Microscopy, MSU) for technical support. Finally, we would sincerely thank the anonymous Reviewers for friendly, detailed and valuable comments and corrections.
This study was supported by grants 18-05-60158 and 16-04-00343 from the Russian Fund for Basic Research (electron microscopy investigations). The field work and sampling were carried out with the financial support of the Joint Vietnam–Russia Tropical Science and Technology Research Center (Ecolan—E3.1 project).
Funding
This study was supported by grants 18–05-60158 and 16–04-00343 from the Russian Fund for Basic Research (electron microscopy investigations). The field work and sampling were carried out with the financial support of the Joint Vietnam–Russia Tropical Science and Technology Research Center (Ecolan—E3.1 project).
Author information
Authors and Affiliations
Contributions
All authors set an aim of the study, collected samples, discussed the results, drafted the work; Elena Mekhova performed measurements, Glafira Kolbasova make SEM photos. All authors approved the version to be published and agreed the be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest/Competing interests
On behalf of all authors, the corresponding author states that there are no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mekhova, E., Nguyen, T.H.T. & Kolbasova, G. First record of tropical myzostomid population size structure and host infestation in Myzostoma khanhkhoaense (Myzostomida: Annelida). Biologia 79, 2143–2150 (2024). https://doi.org/10.1007/s11756-024-01696-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-024-01696-4