Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T16:38:41.171Z Has data issue: false hasContentIssue false
  • English
  • Français

Feeding biology of carnivore and detritivore Mediterranean pycnogonids

Published online by Cambridge University Press:  09 September 2011

Anna Soler-Membrives ,
Claudia P. Arango ,
Montserrat Cuadrado  and
Tomás Munilla
Anna Soler-Membrives*
Affiliation:
Unitat de Zoologia, Facultat de Biociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
Claudia P. Arango
Affiliation:
Queensland Museum, Biodiversity Program, PO Box 3300, South Brisbane, 4101 Qld, Australia
Montserrat Cuadrado
Affiliation:
Unitat de Zoologia, Facultat de Biociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
Tomás Munilla
Affiliation:
Unitat de Zoologia, Facultat de Biociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
*
Correspondence should be addressed to: A. Soler-Membrives, Unitat de Zoologia, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain email: Anna.Soler@uab.cat
Get access Rights & Permissions [Opens in a new window]

Abstract

The digestive system of sea spiders (Pycnogonida) presents peculiarities that have not been discussed in the context of their ecology or feeding behaviour. We investigated the digestive system of two Mediterranean species, a carnivorous species Ammothella longipes and a detritivorous Endeis spinosa, with special focus on its correlation with behavioural feeding habits. The midgut and hindgut sections did not present significant differences between the two species, but major differences were observed in the foregut, reflecting concordance to their diet and their feeding behaviour. Jaws, setose lips, the structure of the pharyngeal filter and musculature of the proboscis are the main differential elements when comparing feeding habits of A. longipes and E. spinosa. These elements are responsible for the reduction of the food pulp down to subcellular size. The digestion process observed in the species studied agrees with that observed in other pycnogonid lineages, but differs from most marine arthropods mainly because of the absence of midgut gland cells and the presence of a unique multifunctional type of midgut epithelial cell. Epithelial digestive cells are present in a small ‘resting’ form during starvation periods. During digestion, secretion granules possibly containing zymogen move to their apical border to be secreted to the midgut lumen, secondary lysosomes are formed and intracellular digestion occurs within them. Residual bodies are formed within the epithelial cell and released to the midgut lumen to be transported towards the hindgut. The characteristics of the digestive process of the pycnogonids studied seem to reflect a plesiomorphic state in arthropods.

Keywords

PycnogonidaMediterranean Seaforegutmidgutfeeding biologycarnivorydetritivorydigestive process
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 3 , May 2013 , pp. 635 - 643
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arango, C.P. (2001) Sea spiders (Pycnogonida) from the Great Barrier Reef, Australia, feed on fire corals and zoanthids. Memoirs of the Queensland Museum 46, 656.Google Scholar
Arango, C.P. (2003) Sea spiders (Arthropoda, Pycnogonida) from the Great Barrier Reef: new species, new records and ecological annotations. Journal of Natural History 37, 2723–2772.CrossRefGoogle Scholar
Arango, C.P. and Brodie, G. (2003) Observations of predation on the tropical nudibranch Okenia sp. by the sea spider Anoplodactylus longiceps Williams (Arthropoda: Pycnogonida). Veliger 46, 99–101.Google Scholar
Arnaud, F. and Bamber, R.N. (1987) The biology of the Pycnogonida. Advances in Marine Biology 24, 1–96.Google Scholar
Bain, B.A. (1991) Some observations on biology and feeding behavior in two southern California pycnogonids. Bijdragen Tot De Dierkunde 61, 63–64.CrossRefGoogle Scholar
Bamber, R.N. (1985) Why do pycnogonids prefer inaccessible anemones? Porcupine Newsletter 3, 67–71.Google Scholar
Barreto, F.S. and Avise, J.C. (2008) Polygynandry and sexual size dimorphism in the sea spider Ammothea hilgendorfi (Pycnogonida: Ammotheidae), a marine arthropod with brood-carrying males. Molecular Ecology 17, 4164–4175.CrossRefGoogle ScholarPubMed
Bilinski, S.M., Szymanska, B. and Miyazaki, K. (2008) Formation of an egg envelope in the pycnogonid, Propallene longiceps (Pycnogonida: Callipallenidae). Arthropod Structure and Development 37, 155–162.CrossRefGoogle ScholarPubMed
Braby, C.E., Pearse, V.B., Bain, B.A. and Vrijenhoek, R.C. (2009) Pycnogonid–cnidarian trophic interactions in the deep Monterey Submarine Canyon. Invertebrate Biology 128, 359–363.CrossRefGoogle Scholar
Brenneis, G., Ungerer, P. and Scholtz, G. (2008) The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment. Evolution and Development 10, 717–724.CrossRefGoogle ScholarPubMed
Dencker, D. (1974) Das Skeletmuskelsystem von Nymphon rubrum Hodge, 1862 (Pycnogonida: Nymphonidae). Zoologische Jahrbücher Abteilung Anatomie 93, 272–287.Google Scholar
Dewel, R.A., Nelson, D.R. and Dewel, W.C. (1993) Tardigrada. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 12: Onychophora, Chilopoda, and lesser Protostomata. New York: Wiley-Liss, pp. 143–183.Google Scholar
Dohrn, A. (1881) Die Pantopoden des Golfes von Neapel und der angrenzenden Meeresabschnitte. Fauna und Flora des Golfes von Neapel 3, 1–252.Google Scholar
Dunlop, J.A. and Arango, C.P. (2005) Pycnogonid affinities: a review. Journal of Zoological Systematics and Evolutionary Research 43, 8–21.CrossRefGoogle Scholar
Fahrenbach, W.H. and Arango, C.P. (2007) Microscopic anatomy of Pycnogonida: II. Digestive system. III. Excretory system. Journal of Morphology 268, 917–935.CrossRefGoogle ScholarPubMed
Felgenhauer, B.E. (1999) Araneae. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 8A: Chelicerate Arthropoda. New York: Wiley-Liss, pp. 223–266.Google Scholar
Filimonova, S.A. (2009) The ultrastructural investigation of the midgut in the quill mite Syringophilopsis fringilla (Acari, Trombidiformes: Syringophilidae). Arthropod Structure and Development 38, 303–313.CrossRefGoogle ScholarPubMed
Fry, W.G. (1965) The feeding mechanism and preferred foods of three species of Pycnogonida. Bulletin of the British Museum of Natural History (Zoology) 12, 197–223.Google Scholar
Harrison, F.W. and Foelix, R.F. (1999) Chelicerate Arthropoda. In Harrison, F.W. and Foelix, R.F. (eds) Microscopic anatomy of invertebrates, Volume 8. Chelicerates. New York: Wiley-Liss, 1116 pp.Google Scholar
Harrison, F.W. and Humes, R.F. (1992) Crustacea. In Harrison, F.W. and Foelix, R.F. (eds) Microscopic anatomy of invertebrates, Volume 9. New York: Wiley-Liss, p. 652.Google Scholar
Helfer, H. and Schlottke, E. (1935) Pantopoda. In Bronns, H.D. (ed.) Klassen Ordnungen Tierreichs. Leipzig: Akademische Verlagsgesellschaft 5, pp. 1–314.Google Scholar
Heß, M. and Melzer, R.R. (2003) Anoplodactylus petiolatus (Pycnogonida) and Hydractinia echinata (Hydrozoa)—observations on galls, feeding behaviour and the host's defence. Vie et Milieu 53, 135–138.Google Scholar
Hoek, P.P.C. (1881) Report on the Pycnogonida dredged by HMS Challenger, during the years 1873–1876. In Report on the scientific results of the voyage of the H.M.S. Challenger during the years 1873–76 3 (Part X), pp. 1–252.Google Scholar
Imandeh, N.G. and King, P.E. (2001) Food and feeding behaviour of Nymphon gracile (Pycnogonida: Nymphonidae) around the Mumbles Pier area of Swansea, United Kingdom. Journal of Aquatic Sciences 16, 33–34.CrossRefGoogle Scholar
King, P.E. (1973) Pycnogonida. London: Hutchinson, 144 pp.Google Scholar
Lotz, G. (1968) Nahrungsaufnahme und Beutefang bei einem Pantopoden, Anoplodactylus Krøyer. Oecologia 1, 171–175.CrossRefGoogle Scholar
Miyazaki, K. (2002) On the shape of foregut lumen in sea spiders (Arthropoda: Pycnogonida). Journal of the Marine Biological Association of the United Kingdom 82, 1037–1038.CrossRefGoogle Scholar
Prell, H. (1909) Beiträge zur Kenntniss der Lebensweise einiger Pantopoden. Bergens Museum Aarbog 10, 3–29.Google Scholar
Regier, J.C., Shultz, J.W., Zwick, A., Hussey, A., Ball, B., Wetzer, R., Martin, J.W. and Cunningham, C.W. (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079.CrossRefGoogle ScholarPubMed
Richards, P.R. and Fry, W.G. (1978) Pycnogonid digestion: a study of some polar forms. Zoological Journal of the Linnean Society 63, 75–97.CrossRefGoogle Scholar
Rogers, C.N., De Nys, R. and Steinberg, P.D. (2000) Predation on juvenile Aplysia parvula and other small anaspidean, sacoglossan, and nudibranch gastropods by pycnogonids. Veliger 43, 330–337.Google Scholar
Russel, D.J. and Hedgpeth, J.W. (1990) Host utilization during ontogeny by two pycnogonid species (Tanystylum duospinum and Ammothea hilgendorfi) parasitic on the hydroid Eucopella everta (Coelenterata, Campanulariidae). Bijdragen Tot De Dierkunde 60, 215–224.Google Scholar
Sanchez, S. (1959) Le développement des Pycnogonides et leurs affinités avec les Arachnides. Archives de Zoologie Expérimentale et Générale 98, 1–102.Google Scholar
Schlottke, E. (1933) Darm und Verdauung bei Pantopoden. Zeitschrift für Mikroskopisch Anatomische Forschung 32, 633–658.Google Scholar
Schmidt-Rhaesa, A. (2007) The evolution of organ systems. Oxford: Oxford University Press.CrossRefGoogle Scholar
Soler-Membrives, A., Rossi, S. and Munilla, T. (2011) Feeding ecology of Ammothella longipes (Pycnogonida): in the Mediterranean sea: a fatty acid biomake approach. Estuarine, Coastal and Shelf Science 92, 588–597.CrossRefGoogle Scholar
Stock, J.H. (1978) Experiments on food preference and chemical sense in Pycnogonida. Zoological Journal of the Linnean Society 63, 59–74.CrossRefGoogle Scholar
Storch, V., Strus, J. and Brandt, A. (2002) Microscopic anatomy and ultrastructure of the digestive system of Natatolana obtusata (Vanhöffen, 1914) (Crustacea, Isopoda). Acta Zoologica 83, 1–14.CrossRefGoogle Scholar
Tomaschko, K.H., Wilhelm, E. and Bückmann, D. (1997) Growth and reproduction of Pycnogonum litorale (Pycnogonida) under laboratory conditions. Marine Biology 129, 595–600.CrossRefGoogle Scholar
Ungerer, P. and Scholtz, G. (2009) Cleavage and gastrulation in Pycnogonum litorale (Arthropoda, Pycnogonida): morphological support for the Ecdysozoa. Zoomorphology 128, 263–274.CrossRefGoogle Scholar
Vilpoux, K. and Waloszek, D. (2003) Larval development and morphogenesis of the sea spider Pycnogonum litorale (Ström, 1762) and the tagmosis of the body of Pantopoda. Arthropod Structure and Development 32, 349–383.CrossRefGoogle ScholarPubMed
Voltzow, J. (1994) Gastropoda Prosobranchia. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 5: Mollusca I. New York: Wiley-Liss, pp. 111–252.Google Scholar
Wirén, E. (1918) Zur Morphologie und Phylogenie der Pantopoden. Zoological Bidrag 6, 41–181.Google Scholar
Wyer, D. and King, P.E. (1974) Feeding in British littoral pycnogonids. Estuarine, Coastal and Marine Science 2, 177–184.CrossRefGoogle Scholar

Soler-Membrives Supplementary Material

Movie

Download Soler-Membrives Supplementary Material(Video)
Video 3.8 MB