COLONY FORM AND THE EXPLOITATION OF SPATIAL REFUGES BY ENCRUSTING BRYOZOA
J. D. D. BISHOP
Departments of Palaeontology and Zoology, British Museum (Natural History), London SW7 5BD
*School of Biological Sciences, University College of Swansea, Swansea SA2 8PP
Search for more papers by this authorJ. D. D. BISHOP
Departments of Palaeontology and Zoology, British Museum (Natural History), London SW7 5BD
*School of Biological Sciences, University College of Swansea, Swansea SA2 8PP
Search for more papers by this authorSummary
The sheet-runner continuum model of unilaminar encrusting colony growth is reassessed for cheilostome Bryozoa. It is concluded that the model does not adequately account for the existence of spatially predictable refuges from mortality, which can be selected by the larva at the time of settlement.
A third end-point category of colony form, named the spot colony, is recognized for species settling in small spatially predictable refuges and growing to small, early maturing colonies of determinate or semi-determinate size. Similar colonies are reported from spatially restrictive substrates such as flexible algal fronds and single sediment grains on particulate seabeds.
Runner growth is also reappraised. In some cases, uniserial growth may be regarded as a primary adaptation for growth in linear refuges, or on maze-like or strongly three-dimensional surfaces where multiserial growth is impossible, rather than as a general fugitive strategy adopted by competitively inferior forms.
A revised classificatory model for encrusting growth is proposed. This consists of two continua, sheet-ribbon-runner and sheet-patch-spot. It is suggested that an improved ecological classification of encrusting growth might be framed as a series of coupled settlement/growth strategies.
References
- Arístegui, J. (1987) Introducción al estudio de las comunidades de briozoos mas representativas del literal de las Islas Canarias. Cahiers de Biologie Marine 28, 323–338.
- Banta, W. C. (1976) Origin and early evolution of cheilostome Bryozoa. Documents des Laboratoires de Géologie de la FacØlté des Sciences de Lyon, Hors Série 3, 565–582.
- Bernstein, B. B. & Jung, N. (1979) Selective pressures and coevolution in a kelp canopy community in southern California. Ecological Monographs 49, 335–355.
- Bishop, J. D. D. (1988) Disarticulated bivalve shells as substrates for encrustation by the bryozoan Cribrilina puncturata in the Plio-Pleistocene Red Crag of eastern England. Palaeontology 31, 237–253.
- Boardman, R. S., Cheetham, A. H., Oliver, W. A., Jr., Coates, A. G. & Bayer, F. M. (1973) Introducing coloniality. In Animal Colonies. Development and Function Through Time (ed. R. S. Boardman, A. H. Cheetham and W. A. Oliver), pp. v–ix. Dowden , Hutchinson & Ross Stroudsburg .
- Buss, L. W. (1979) Habitat selection, directional growth and spatial refuges: why colonial animals have more hiding places. In Biology and Systematics of Colonial Organisms (ed. G. Larwood and B. R. Rosen), pp. 459–497. Academic Press, London , New York .
- Buss, L. W. (1980) Competitive intransitivity and size-frequency distributions of interacting populations. Proceedings of the National Academy of Sciences of the USA 77, 5355–5359.
- Buss, L. W. (1986) Competition and community organization on hard surfaces in the sea. In Community Ecology (ed. J. Diamond and T. J. Case), pp. 517–536. Harper & Row, New York .
- Cancino, J. M. (1986) Marine macroalgae as a substratum for sessile invertebrates: a study of Celleporella hyalina (Bryozoa) on fronds of Laminaria saccharina (Phaeophyta). Monographías Bioldgicas 4, 279–308.
- Cancino, J. M. & Hughes, R. N. (1987) The effect of water flow on growth and reproduction of Celleporella hyalina (L.) (Bryozoa: Cheilostomata). Journal of Experimental Marine Biology and Ecology 112, 109–130.
- Cheetham, A. H. (1986) Branching, biomechanics and bryozoan evolution. Proceedings of the Royal Society of London, Series B 228, 151–171.
- Cheetham, A. H. & Hayek, L.-A. C. (1983) Geometric consequences of branching growth in adeoniform Bryozoa. Paleobiology 9, 240–260.
- Coates, A. G. & Jackson, J. B. C. (1985) Morphological themes in the evolution of clonal and aclonal marine invertebrates. In Population Biology and Evolution of Clonal Organisms (ed. J. B. C. Jackson, L. W. Buss and R. E. Cook), pp. 67–106. Yale University Press, New Haven .
- Cook, P. L. (1985) Bryozoa from Ghana, a preliminary survey. (Annates, Musée Royal de l'Afrique Centrale, Sciences Zoologiques 238, 1–315.
- Cook, P. L. & Chimonides, P. J. (1984) Recent and fossil Lunulitidae (Bryozoa: Cheilostomata) 2. Species of Helixotionella gen. nov. from Australia. Journal of Natural History 18, 255–270.
- Gordon, D. P. (1984) The marine fauna of New Zealand: Bryozoa: Gymnolaemata from the Kermadec Ridge. New Zealand Oceanographic Institute Memoir 91, 1–198.
- Håkansson, E. & Winston, J. E. (1985) Interstitial bryozoans: unexpected life forms in a high energy environment. In Bryozoa: Ordovician to Recent (ed. C. Nielsen and G. P. Larwood), pp. 125–134. Olsen & Olsen, Fredensborg .
- Harmelin, J. G. (1977) Bryozoaires du banc de la Conception (nord des Canaries) Campagne Cineca I du ‘Jean Charcot’. Bulletin du Museum National d'Histoire Naturelle, 3e Série, Zoology 341, 1057–1076.
- Harmelin, J. G. (1985) Bryozoan dominated assemblages in Mediterranean cryptic environments. In Bryozoa: Ordovician to Recent (ed. C. Nielsen and G. P. Larwood), pp. 135–143. Olsen & Olsen, Fredensborg .
- Harmelin, J. G. (1986) Patterns in the distribution of bryozoans in the Mediterranean marine caves. Stygologia 2, 10–25.
- Harmer, S. F. (1926) The Polyzoa of the Siboga Expedition. Part II. Cheilostomata Anasca. Siboga-Expeditie 28b, 181–501.
- Hayward, P. J. (1980) Cheilostomata (Bryozoa) from the South Atlantic. Journal of Natural History 14, 701–722.
- Hayward, P. J. & Cook, P. L. (1979) The South African Museum's Meiring Naude Cruises, Part 9. Bryozoa. Annals of the South African Museum 79, 43–130.
- Hayward, P. J. & Fordy, M. R. (1982) Anew species of bryozoan epizooite from South Africa. Journal of Natural History 16, 769–773.
- Hayward, P. J. & Ryland, J. S. (1979) British ascophoran bryozoans. Synopses of the British Fauna, New Series 14, 1–312.
- Hughes, D.J. & Hughes, R. N. (1986) Metabolic implications of modularity: studies on the respiration and growth of Electra pilosa. Philosophical Transactions of the Royal Society of London, Series B 313, 23–29.
- Hughes, R. N. (1987) The functional ecology of clonal animals. Functional Ecology 1, 63–69.
- Hughes, R. N. & Cancino, J. M. (1985) An ecological overview of cloning in Metazoa. In Population Biology and Evolution of Clonal Organisms (ed. J. B. C. Jackson, L. W. Buss & R. E. Cook), pp. 153–186. Yale University Press, New Haven .
- Hughes, T. P. (1984) Population dynamics based on individual size rather than age: a general model with a reef coral example. American Naturalist 123, 778–795.
- Illies, G. (1976) On the genus Stomatoporina Balavoine, 1958 (Bryozoa Cyclostomata). Documents des Laboratoires de Géologie de la Faculté des Sciences de Lyon, Hors Série 3, 51–57.
- Jackson, J. B. C. (1977a) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. American Naturalist 111, 743–767.
- Jackson, J. B. C. (1977b) Growth form, zooid morphology and evolutionary rates of marine colonial animals. Journal of Paleontology 51, (pt 2, suppl. 3), 16.
- Jackson, J. B. C. (1979a) Morphological strategies of sessile animals. In Biology and Systematics of Colonial Organisms (ed. G. Larwood and B. R. Rosen), pp. 499–555. Academic Press, London , New York .
- Jackson, J. B. C. (1979b) Overgrowth competition between encrusting cheilostome ectoprocts in a Jamaican cryptic reef environment. Journal of Animal Ecology 48, 805–823.
- Jackson, J. B. C. (1981) Competitive interactions between bryozoans and other organisms. In Lophophorates. Notes for a Short Course (ed. J. T. Dutro, and R. S. Boardman), pp. 22–36. University of Tennessee, Knoxville .
-
Jackson, J. B. C. (1983) Biological determinants of present and past sessile animal distributions. In Biotic Interactions in Recent and Fossil Benthic Communities (ed.
M. J. S. Tevesz and
P. L. McCall), pp. 39–120. Plenum,
New York
.
10.1007/978-1-4757-0740-3_2 Google Scholar
- Jackson, J. B. C. (1985) Distribution and ecology of clonal and aclonal benthic invertebrates. In Population Biology and Evolution of Clonal Organisms (ed. J. B. C. Jackson, L. W. Buss and R. E. Cook), pp. 297–355. Yale University Press, New Haven .
- Jackson, J. B. C. & Coates, A. G. (1986) Life cycles and evolution of clonal (modular) animals. Philosophical Transactions of the Royal Society of London, Series B 313, 7–22.
- Jackson, J. B. C. & Hughes, T. P. (1985) Adaptive strategies of coral-reef invertebrates. American Scientist 73, 265–274.
- Jackson, J. B. C. & Wertheimer, S. P. (1985) Patterns of reproduction in five common species of Jamaican reef-associated bryozoans. In Bryozoa: Ordovician to Recent (ed. C. Nielsen and G. P. Larwood), pp. 161–168. Olsen & Olsen, Fredensborg .
- Jackson, J. B. C. & Winston, J. E. (1981) Modular growth and longevity in bryozoans. In Recent and Fossil Bryozoa (ed. G. P. Larwood and C. Nielsen), pp. 121–126. Olsen & Olsen, Fredensborg .
- Jebram, D. (1980) Influences of the food on the colony forms of Electra pilosa (Bryozoa, Cheilostomata). Zoologische Jahrbucher, Systematik 108, 1–14.
- Jebram, D. & Rummert, H.-D. (1978) Influences of different diets on growth and forms of Conopeum seurati (Canu) (Bryozoa, Cheilostomata). Zoologische Jahrbücher, Systematik 105, 502–514.
- Jullien, J. (1883) Dragages du Travailleur. Bryozoaires. Espèces draguées dans l'Ocean Atlantique en 1881. Bulletin de la Société Zoologique de France 7, 497–529.
- Keough, M. J. & Downes, B. J. (1982) Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia 54, 348–352.
- Lagaaij, R. (1963) New additions to the bryozoan fauna of the Gulf of Mexico. Publications of the Institute of Marine Science, University of Texas 9, 162–236.
- Larwood, G. P. & Taylor, P. D. (1979) Early structural and ecological diversification in the Bryozoa. In The Origin of Major Invertebrate Groups (ed. M. R. House), pp. 209–234. Academic Press, London , New York .
- Lidgard, S. (1985) Zooid and colony growth in encrusting cheilostome bryozoans. Palaeontology 28, 255–291.
- Lutaud, G. (1961) Contribution a l‘étude du bourgeonnement et de la croissance des colonies chez Membranipora membranacea (Linné), bryozoaire chilostome. Annates de la Société Royale Zoologique de Belgique 91, 157–300.
-
MacArthur, R. H. &
Wilson, E. O. (1967) The Theory of Island Biogeography. Princeton University Press,
Princeton
.
10.1111/j.1463-6409.2007.00280.x Google Scholar
- McKinney, F. K. (1988) Exploitation of Cornucopina tuba (Bryozoa: Cheilostomata) by Aetea curta (Bryozoa: Cheilostomata). Journal of Natural History 22, 1545–1549.
- Pianka, E. R. (1970) On r- and K-selection. American Naturalist 104, 592–596.
- Pohowsky, R. A. (1973) A Jurassic cheilostome from England. In Living and Fossil Bryozoa (ed. G. P. Larwood), pp. 447–461. Academic Press, London .
- Ridley, M. (1986) Evolution and Classification. The Reformation of Cladism. Longman, London , New York .
- Ross, J. R. P. (1979) Ectoproct adaptations and ecological strategies. In Advances in Bryozoology (ed. G. P. Larwood and M. B. Abbott), pp. 283–294. Academic Press, London , New York .
- Rubin, J. A. (1987) Growth and refuge location in continuous, modular organisms: experimental and computer simulation studies. Oecologia 72, 46–51.
- Ryland, J. S. (1959) Experiments on the selection of algal substrates by polyzoan larvae. Journal of Experimental Biology 36, 613–631.
- Ryland, J. S. & Gordon, D. P. (1977) Some New Zealand and British species of Hippothoa (Bryozoa: Cheilostomata). Journal of the Royal Society of New Zealand 7, 7, 49.
- Ryland, J. S. & Hayward, P. J. (1977) British anascan bryozoans. Synopses of the British Fauna, New Series 10, 1–188.
- Ryland, J. S. & Stebbing, A. R. D. (1971) Settlement and orientated growth in epiphytic and epizoic bryozoans. In Fourth European Marine Biology Symposium (ed. D. J. Crisp), pp. 105–123. Cambridge University Press, Cambridge .
- Sackville Hamilton, N. R., Schmid, B. & Harper, J. L. (1987) Life-history concepts and the population biology of clonal organisms. Proceedings of the Royal Society of London, Series B 232, 35–57.
- Schopf, T. J. M. (1977) Patterns and themes of evolution among the Bryozoa. In Patterns of Evolution (ed. A. Hallam), pp. 159–207. Elsevier, Amsterdam .
- Silén, L. (1942) On spiral growth of the zoaria of certain Bryozoa. Arkiv för Zoologi 34 A, 1–22.
- Silén, L. (1944) On the formation of the interzoidal communications of the Bryozoa. Zoologiska Bidrag från Uppsala 22, 433–488.
- Silén, L. (1987) Colony growth pattern in Electra pilosa (Linnaeus) and comparable encrusting cheilostome bryozoans. Acta Zoologica 68, 17–34.
- Silén, L. & Harmelin, J. G. (1976) Haplopoma sciaphilum sp.n., a cave-living bryozoan from the Skagerrak and the Mediterranean. Zoologica Scripta 5, 61–66.
- Simma-Krieg, B. (1969) On the variation and special reproduction habits of Aetea sica (Couch). Cahiers de Biologie Marine 10, 129–137.
- Stebbing, A. R. D. (1973) Competition for space between the epiphytes of Fucus serratus L. Journal of the Marine Biological Association of the United Kingdom 53, 247–261.
- Taylor, P. D. (1979) Functional significance of contrasting colony form in two Mesozoic encrusting bryozoans. Palaeogeography, Palaeoclimatology, Palaeoecology 26, 151–158.
- Taylor, P. D. (1984) Adaptations for spatial competition and utilization in Silurian encrusting bryozoans. Special Papers in Palaeontology 32, 197–210.
- Taylor, P. D. (1986) Charixa Lang and Spinicharixa gen. nov., cheilostome bryozoans from the Lower Cretaceous. Bulletin of the British Museum (Natural History), Geology 40, 197–222.
- Taylor, P. D. (1988) Colony growth pattern and astogenetic gradients in the Cretaceous cheilostome bryozoan Herpetopora. Palaeontology 31, 519–549.
- Thorpe, J. P. & Ryland, J. S. (1987) Some theoretical limitations on the arrangement of zooids in encrusting Bryozoa. In Bryozoa: Present and Past (ed. J. R. P. Ross), pp. 277–283. Western Washington University, Bellingham .
- Voigt, E. (1987) Thalassinoid burrows in the Maastrichtian Chalk Tuff near Maastricht (The Netherlands) as a fossil hardground microcavern biotope of Cretaceous Bryozoans. In Bryozoa: Present and Past (ed. J. R. P. Ross), pp. 293–300. Western Washington University, Bellingham .
- Voigt, E. & Hillmer, G. (1983) Oberkretazische Hippothoidae (Bryozoa Cheilostomata) aus dem Campanium von Schweden und dem Maastrichtium der Niederlande. Mitteilungen aus dem Geologisch-Palaontologischen Institut der Universität Hamburg 54, 169–208.
- Winston, J. E. (1976) Experimental culture of the estuarine ectoproct Conopeum tenuissimum from Chesapeake Bay. Biological Bulletin 150, 318–335.
- Winston, J. E. (1981) Life histories of colonial invertebrates. Paleobiology 7, 151–153.
- Winston, J. E. (1982) Marine bryozoans (Ectoprocta) of the Indian River area (Florida). Bulletin of the American Museum of Natural History 173, 99–176.
- Winston, J. E. (1985) Life history studies of Disporella and Drepanophora in Jamaica. In Bryozoa: Ordovician to Recent (ed. C. Nielsen and G. P. Larwood), p. 350. Olsen & Olsen, Fredensborg .
- Winston, J. E. & Eiseman, N. J. (1980) Bryozoan-algal associations in coastal and continental shelf waters of eastern Florida. Florida Scientist 43, 65–74.
- Winston, J. E. & Håkansson, E. (1986) The interstitial bryozoan fauna from Capron Shoal, Florida. American Museum Novitates 2865, 1–50.
- Winston, J. E. & Jackson, J. B. C. (1984) Ecology of cryptic coral reef communities. IV. Community development and life histories of encrusting cheilostome Bryozoa. Journal of Experimental Marine Biology and Ecology 76, 1–21.
- Woodin, S. A. & Jackson, J. B. C. (1979) Interphyletic competition among marine benthos. American Zoologist 19, 1029–1043.
- Yoshioka, P. M. (1982) Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology 63, 457–468.