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.
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
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
Collins AG, Valentine JW (2001) Defining phyla: evolutionary pathways to animal body plans. Evol Dev 36:432–442
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
Cotte J (1903) Contribution à l’étude de la nutrition chez les spongiaires. Bull Sci Fr Belg 38:420–573
Dewel RA (2000) Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. J Morphol 243:35–74
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
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
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
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
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
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
Monniot C (1984) Les invertébrés suspensivores: adaptations à un régime carnivore chez les Tuniciers. Oceanis 10:605–621
Monniot C, Monniot F (1975) Abyssal tunicates: an ecological paradox. Ann Inst Oceanogr 51:99–129
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
Passelaigue F, Bourdillon A (1986) Distribution and circadian migrations of the cavernicolous mysid Hemimysis speluncola Ledoyer. Stygologia 2:112–118
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
Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591
Schmidt I (1970) Phagocytose et pinocytose chez les Spongillidae. Z Vergl Physiol 66:398–420
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
Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature 373:333–335
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
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
Vooren CM (1973) A note on the occurrence of small fishes in sponges. Tuatara 20:109–112
Willenz P, Van de Vyver G (1984) Ultrastructural localization of lysosomal digestion in the freshwater sponge Ephydatia fluviatilis. J Ultrastruct Res 87:13–22
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
Corresponding author
Electronic Supplementary Material
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-004-0100-0