Zoomorphology

, Volume 123, Issue 4, pp 179–190 | Cite as

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

Original Article

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.

Keywords

Porifera Carnivory Asbestopluma Feeding process Ultrastructure Deep-sea Evolution of Metazoa 

Supplementary material

Video (extracted from Vacelet J (1998) Carnivorous sponge. Video, CNRS Audiovisuel, 13 min). Animation from time lapse photographs (interval shots 3 h over a ten day period) of the digestion of a mysid shrimp Hemimysis speluncola by the carnivorous sponge Asbestopluma hypogea

video.zip (860 kb)
video.zip (MPG format, 3.6 MB)

References

  1. Aristotle (350 BC) History of animals (translated by D’Arcy Wentworth Thompson). http://www.4literature.net/Aristotle/History_of_Animals/
  2. Bergquist PR (1978) Sponges. Hutchinson, LondonGoogle Scholar
  3. 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 14:171–179CrossRefGoogle Scholar
  4. Cheng TC, Yee HWF, Rifkin E, Kramer M (1968) Cellular reactions in Terpios zeteki to implanted heterologous biological materials. J Invert Pathol 12:29–35Google Scholar
  5. Collins AG, Valentine JW (2001) Defining phyla: evolutionary pathways to animal body plans. Evol Dev 36:432–442CrossRefGoogle Scholar
  6. Connes R, Paris J, Sube J (1971) Réactions tissulaires de quelques démosponges vis à vis de leurs commensaux et parasites. Naturaliste Can 98:923–935Google Scholar
  7. Cotte J (1903) Contribution à l’étude de la nutrition chez les spongiaires. Bull Sci Fr Belg 38:420–573Google Scholar
  8. Dewel RA (2000) Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. J Morphol 243:35–74CrossRefPubMedGoogle Scholar
  9. 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 13–27Google Scholar
  10. Hahn-Keser B, Stockem W (1997) Detection of distinct endocytotic and phagocytotic activities in epithelial cells (pinacocytes) of freshwater sponges (Porifera, Spongillidae). Zoomorphology 117:121–134CrossRefGoogle Scholar
  11. Hahn-Keser B, Stockem W (1998) Intracellular pathways and degradation of endosomal contents in basal epithelial cells of freshwater sponges (Porifera, Spongillidae). Zoomorphology 117:223–236CrossRefGoogle Scholar
  12. 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 636–641Google Scholar
  13. 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 1–3Google Scholar
  14. 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 18:112–116Google Scholar
  15. Koltun VM (1970) Sponge fauna of the north-western Pacific from the shallows to the ultra-abyssal depths. Inst Oceanol Acad Sci USSR 86:165–221Google Scholar
  16. 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 44:289–298Google Scholar
  17. 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 98:9707–9712PubMedGoogle Scholar
  18. Monniot C (1984) Les invertébrés suspensivores: adaptations à un régime carnivore chez les Tuniciers. Oceanis 10:605–621Google Scholar
  19. Monniot C, Monniot F (1975) Abyssal tunicates: an ecological paradox. Ann Inst Oceanogr 51:99–129Google Scholar
  20. 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 312:383–388Google Scholar
  21. Passelaigue F, Bourdillon A (1986) Distribution and circadian migrations of the cavernicolous mysid Hemimysis speluncola Ledoyer. Stygologia 2:112–118Google Scholar
  22. 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 319:385–391Google Scholar
  23. Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591Google Scholar
  24. Schmidt I (1970) Phagocytose et pinocytose chez les Spongillidae. Z Vergl Physiol 66:398–420Google Scholar
  25. Simpson TL (1984) The cell biology of sponges. Springer, Berlin Heidelberg New YorkGoogle Scholar
  26. Tuzet O, Paris J (1964) Réactions tissulaires de l’éponge Suberites domuncula (Olivi) Nardo, vis-à-vis de ses commensaux et parasites. Vie Milieu 17:147–155Google Scholar
  27. Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature 373:333–335Google Scholar
  28. 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):109–115Google Scholar
  29. Vacelet J, Boury-Esnault N, Harmelin JG (1994) Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep-Sea Res 41:965–973Google Scholar
  30. Vooren CM (1973) A note on the occurrence of small fishes in sponges. Tuatara 20:109–112Google Scholar
  31. Willenz P, Van de Vyver G (1984) Ultrastructural localization of lysosomal digestion in the freshwater sponge Ephydatia fluviatilis. J Ultrastruct Res 87:13–22Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Centre d’Océanologie de Marseille (CNRS-Université de la Méditerranée, UMR 6540 DIMAR)Station Marine d’EndoumeMarseilleFrance

Personalised recommendations