Skip to main content
Log in

Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae)

  • Original Article
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

Asbestopluma hypogea (Porifera) is a carnivorous species that belongs to the deep-sea taxon Cladorhizidae but lives in littoral caves and can be raised easily in an aquarium. It passively captures its prey by means of filaments covered with hook-like spicules. Various invertebrate species provided with setae or thin appendages are able to be captured, although minute crustaceans up to 8 mm long are the most suitable prey. Transmission electron microscopy observations have been made during the digestion process. The prey is engulfed in a few hours by the sponge cells, which migrate from the whole body towards the prey and concentrate around it. A primary extracellular digestion possibly involving the activity of sponge cells, autolysis of the prey and bacterial action results in the breaking down of the prey body. Fragments of the prey, including connective cells and muscles, are then phagocytosed and digested by archaeocytes and bacteriocytes. The whole process takes 8–10 days for a large prey. This unique feeding habit implies the capture and digestion of a macro-prey without any digestive cavity. It would appear to be an adaptation to life in deep-sea oligotrophic environments. Carnivorous sponges provide actual evidence, through a functional example, that a transition is possible from the filter-feeder poriferan body plan towards a different organizational plan through loss of the aquiferous system, a transition that has been hypothesized for the early evolution of Metazoa.

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. 1a–f
Fig. 2a, b
Fig. 3a–g
Fig. 4a–f
Fig. 5a–f
Fig. 6a–d

Similar content being viewed by others

References

  • Aristotle (350 BC) History of animals (translated by D’Arcy Wentworth Thompson). http://www.4literature.net/Aristotle/History_of_Animals/

  • Bergquist PR (1978) Sponges. Hutchinson, London

  • Borchiellini C, Manuel M, Alivon E, Boury-Esnault N, Vacelet J, Le Parco Y (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179

    Article  Google Scholar 

  • Cheng TC, Yee HWF, Rifkin E, Kramer M (1968) Cellular reactions in Terpios zeteki to implanted heterologous biological materials. J Invert Pathol 12:29–35

    Google Scholar 

  • Collins AG, Valentine JW (2001) Defining phyla: evolutionary pathways to animal body plans. Evol Dev 36:432–442

    Article  Google Scholar 

  • Connes R, Paris J, Sube J (1971) Réactions tissulaires de quelques démosponges vis à vis de leurs commensaux et parasites. Naturaliste Can 98:923–935

    Google Scholar 

  • Cotte J (1903) Contribution à l’étude de la nutrition chez les spongiaires. Bull Sci Fr Belg 38:420–573

    Google Scholar 

  • Dewel RA (2000) Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. J Morphol 243:35–74

    Article  CAS  PubMed  Google Scholar 

  • Grell KG, Ruthmann A (1991) Placozoa. In: Harrison FW (eds) Microscopic anatomy of invertebrates, vol 2. Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley-Liss, New York, pp 13–27

  • Hahn-Keser B, Stockem W (1997) Detection of distinct endocytotic and phagocytotic activities in epithelial cells (pinacocytes) of freshwater sponges (Porifera, Spongillidae). Zoomorphology 117:121–134

    Article  Google Scholar 

  • Hahn-Keser B, Stockem W (1998) Intracellular pathways and degradation of endosomal contents in basal epithelial cells of freshwater sponges (Porifera, Spongillidae). Zoomorphology 117:223–236

    Article  Google Scholar 

  • Hajdu E, Vacelet J (2002) Family Cladorhizidae. In: Hooper JNA, Soest RWM van (eds) Systema Porifera: a guide to the classification of sponges, vol 1. Kluwer Academic/Plenum, New York, pp 636–641

  • Hooper JNA, Soest RWM van (2002) Introduction. In: Hooper JNA, Soest RWM van (eds) Systema Porifera: a guide to the classification of sponges, vol 1. Kluwer Academic/Plenum, New York, pp 1–3

  • Ivanova EP, Bakunina IY, Gorshkova NM, Romanenko LA, Mikhailov VV, Elyakova LA, Parfenova VV (1993) Occurrence of chitin-decomposing enzymes in marine and freshwater microorganisms. Russ J Mar Biol 18:112–116

    Google Scholar 

  • Koltun VM (1970) Sponge fauna of the north-western Pacific from the shallows to the ultra-abyssal depths. Inst Oceanol Acad Sci USSR 86:165–221

    Google Scholar 

  • Kübler B, Barthel D (1999) A carnivorous sponge, Chondrocladia gigantea (Porifera: Demospongiae: Cladorhizidae), the giant deep-sea clubsponge from the Norwegian trench. Mem Queensl Mus 44:289–298

    Google Scholar 

  • Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypothesis of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci U S A 98:9707–9712

    CAS  PubMed  Google Scholar 

  • Monniot C (1984) Les invertébrés suspensivores: adaptations à un régime carnivore chez les Tuniciers. Oceanis 10:605–621

    Google Scholar 

  • Monniot C, Monniot F (1975) Abyssal tunicates: an ecological paradox. Ann Inst Oceanogr 51:99–129

    Google Scholar 

  • Monniot C, Monniot F (1991) Découverte d’une nouvelle lignée évolutive chez les ascidies de grande profondeur: une Ascidiidae carnivore. C R Acad Sci Paris 312:383–388

    Google Scholar 

  • Passelaigue F, Bourdillon A (1986) Distribution and circadian migrations of the cavernicolous mysid Hemimysis speluncola Ledoyer. Stygologia 2:112–118

    Google Scholar 

  • Perez T (1996) La rétention de particules par une éponge hexactinellide, Oopsacas minuta (Leucopsacasidae): le rôle du réticulum. Particle uptake by a hexactinellid sponge, Oopsacas minuta (Leucopsacasidae): the role of the reticulum. C R Acad Sci Paris 319:385–391

    Google Scholar 

  • Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591

    Google Scholar 

  • Schmidt I (1970) Phagocytose et pinocytose chez les Spongillidae. Z Vergl Physiol 66:398–420

    Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer, Berlin Heidelberg New York

  • Tuzet O, Paris J (1964) Réactions tissulaires de l’éponge Suberites domuncula (Olivi) Nardo, vis-à-vis de ses commensaux et parasites. Vie Milieu 17:147–155

    Google Scholar 

  • Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature 373:333–335

    CAS  Google Scholar 

  • Vacelet J, Boury-Esnault N (1996) A new species of carnivorous sponge (Demospongiae: Cladorhizidae) from a Mediterranean cave. Bull Inst R Sci Nat Belg 66(suppl):109–115

    Google Scholar 

  • Vacelet J, Boury-Esnault N, Harmelin JG (1994) Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep-Sea Res 41:965–973

    Google Scholar 

  • Vooren CM (1973) A note on the occurrence of small fishes in sponges. Tuatara 20:109–112

    Google Scholar 

  • Willenz P, Van de Vyver G (1984) Ultrastructural localization of lysosomal digestion in the freshwater sponge Ephydatia fluviatilis. J Ultrastruct Res 87:13–22

    Google Scholar 

Download references

Acknowledgements

We thank Chantal Bézac for technical assistance, and the Institut de Biologie du Développement, Université de la Méditerranée for giving access to the electron microscopy service. We are also indebted to Laetitia De Jong-Moreau and Roxanne Barthélémy for providing useful advice for the interpretation of crustacean structures, and to Nicole Boury-Esnault for constructive discussions. The experiments comply with the current laws of France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jean Vacelet.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vacelet, J., Duport, E. Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae). Zoomorphology 123, 179–190 (2004). https://doi.org/10.1007/s00435-004-0100-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-004-0100-0

Keywords

Navigation