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Colonies as dynamic systems: reconstructing the life history of Cribrilina annulata (Bryozoa) on two algal substrates

Published online by Cambridge University Press:  14 May 2019

Uliana A. Nekliudova ,
Ksenia V. Shunkina ,
Alexey V. Grishankov ,
Marina A. Varfolomeeva ,
Andrey I. Granovitch  and
Andrew N. Ostrovsky Open the ORCID record for Andrew N. Ostrovsky [Opens in a new window]
Uliana A. Nekliudova
Affiliation:
Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria Department of Invertebrate Zoology, Faculty of Biology, St Petersburg State University, Universitetskaja nab. 7/9, 199034, St Petersburg, Russia
Ksenia V. Shunkina
Affiliation:
Laboratory of Evolutionary Morphology, Zoological Institute, Russian Academy of Sciences, Universitetskaja nab. 1, 199034, St Petersburg, Russia
Alexey V. Grishankov
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, St Petersburg State University, Universitetskaja nab. 7/9, 199034, St Petersburg, Russia
Marina A. Varfolomeeva
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, St Petersburg State University, Universitetskaja nab. 7/9, 199034, St Petersburg, Russia
Andrey I. Granovitch
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, St Petersburg State University, Universitetskaja nab. 7/9, 199034, St Petersburg, Russia
Andrew N. Ostrovsky*
Affiliation:
Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria Department of Invertebrate Zoology, Faculty of Biology, St Petersburg State University, Universitetskaja nab. 7/9, 199034, St Petersburg, Russia
*
Author for correspondence: Andrew N. Ostrovsky, E-mail: [email protected] and [email protected]
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Abstract

Quantifying interconnected performances of the modules in a colonial organism (feeding, sexual reproduction, rejuvenation, dormancy) into an integral picture enables studying functional dynamics and resource allocation at different levels – from module to population. Testing this approach on the common boreal-Arctic bryozoan Cribrilina annulata in the White Sea, we describe its life history, comparing colonies on two algal substrates with contrasting size and lifespan. Colonies living on kelps were much larger and had a higher proportion of dormant zooids, whereas the percentage of reproducing, feeding and rejuvenating zooids was higher in colonies on red algae (with the colonies also exhibiting longer reproductive period). Colony lifespan was dependent both on substrate type and on time of colony establishment, lasting from 4–5 to up to 17 months on kelps and 14–18 months on red algae. During the reproductive season (May–September) the C. annulata population consisted of colonies of three cohorts on both substrata: overwintered and two summer generations that behaved differently. Whereas overwintered and summer colonies established in June–early August produced larvae, most of the colonies established after mid-summer were preparing for hibernation and postponed reproduction until next spring. Moreover, young reproducing colonies formed brooding hermaphrodite zooids of ordinary size, whereas overwintered colonies budded smaller-sized basal and frontal (dwarf) hermaphrodites. Finally, overall zooidal performance in co-existing colonies of the overwintered and young generations was different on kelps, but similar on red algae. Altogether our findings indicate that the life histories of colonial epibionts are much more complex and evolutionarily flexible than generally acknowledged.

Keywords

Modular invertebratelife historyresource allocationsexual reproduction
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 6 , September 2019 , pp. 1363 - 1377
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

AlgaeBase (2018) Available at https://algaebase.org/.Google Scholar
Barnes, DKA and Clarke, A (1995) Seasonality of feeding activity in Antarctic suspension feeders. Polar Biology 15, 335–340.10.1007/BF00238483Google Scholar
Barnes, DKA and Clarke, A (1998) Seasonality of polypide recycling and sexual reproduction in some erect Antarctic bryozoans. Marine Biology 131, 647–658.10.1007/s002270050357Google Scholar
Bernstein, BB and Jung, N (1979) Selective pressure and coevolution in a kelp canopy community in southern California. Ecological Monographs 49, 335–355.10.2307/1942488Google Scholar
Best, MA and Thorpe, JP (1985) Autoradiographic study of feeding and the colonial transport of metabolites in the marine bryozoan Membranipora membranacea. Marine Biology 84, 295–300.10.1007/BF00392499Google Scholar
Best, MA and Thorpe, JP (2001) Use of radioactive labelled food to assess the role of the funicular system in the transport of metabolites in the cheilostome bryozoan Membranipora membranacea (L.). In Wyse Jackson, PN, Buttler, CJ and Spencer Jones, ME (eds), Bryozoan Studies 2001. Lisse: Balkema A.A., pp. 29–35.Google Scholar
Borg, F (1947) Zur Kenntnis der Ökologie und des Lebenszyklus von Electra crustulenta. Zoologiska Bidrag från Uppsala 25, 344–377.Google Scholar
Cadman, PS and Ryland, JS (1996) The characters, reproduction, and growth of Alcyonidium mytili Dalyell, 1848 (Ctenostomatida). In Gordon, DP, Smith, AM and Grant-Mackie, JA (eds), Bryozoans in Space and Time. Wellington: National Institute of Water and Atmospheric Research, pp. 237–242.Google Scholar
Cancino, JM (1986) Marine macroalgae as a substratum for sessile invertebrates: a study of Celleporella hyalina (Bryozoa) on fronds of Laminaria saccharina (Phaeophyta). Monographías Biológicas 4, 279–308.Google Scholar
Cancino, JM and Hughes, RN (1987) The effect of water flow on growth and reproduction of Celleporella hyalina (L.) (Bryozoa: Cheilostomata). Journal of Experimental Marine Biology and Ecology 112, 109–131.10.1016/0022-0981(87)90112-2Google Scholar
Cancino, JM and Hughes, RN (1988) The zooidal polymorphism and astogeny of Celleporella hyalina (Bryozoa: Cheilostomata). Journal of Zoology 215, 167–181.10.1111/j.1469-7998.1988.tb04891.xGoogle Scholar
Conolly, NJ and Drew, EA (1985) Physiology of Laminaria. Marine Ecology 6, 299–320.10.1111/j.1439-0485.1985.tb00139.xGoogle Scholar
Corrêa, DD (1948) A embryologia de Bugula flabellata (J. V. Thompson) Bryozoa Ectoprocta. Boletim da Faculdade de Filosofia, Ciênsias e Letras, Universidade de São Paulo, Zoologia 13, 7–71.Google Scholar
Dudley, JE (1973) Observations on the reproduction, early larval development, and colony astogeny of Conopeum tenuissimum (Canu). Chesapeake Science 14, 270–278.10.2307/1350755Google Scholar
Dyrynda, PEJ (1981) A preliminary study of patterns of polypide generation- degeneration in marine cheilostome Bryozoa. In Larwood, GP and Nielsen, C (eds), Recent and Fossil Bryozoa. Fredensborg: Olsen & Olsen, pp. 73–81.Google Scholar
Dyrynda, PEJ and King, PE (1982) Sexual reproduction in Epistomia bursaria (Bryozoa: Cheilostomata), an endozooidal brooder without polypide recycling. Journal of Zoology 198, 337–352.10.1111/j.1469-7998.1982.tb02080.xGoogle Scholar
Dyrynda, PEJ and King, PE (1983) Gametogenesis in placental and non-placental ovicellate cheilostome Bryozoa. Journal of Zoology 200, 471–492.10.1111/j.1469-7998.1983.tb02810.xGoogle Scholar
Dyrynda, PEJ and Ryland, JS (1982) Reproductive strategies and life histories in the cheilostome marine bryozoans Chartella papyracea and Bugula flabellata. Marine Biology 71, 241–256.10.1007/BF00397041Google Scholar
Eggleston, D (1963) The Marine Polyzoa of the Isle of Man (PhD Thesis). University of Liverpool, England.Google Scholar
Eggleston, D (1972) Patterns of reproduction in the marine Ectoprocta of the Isle of Man. Journal of Natural History 6, 31–38.10.1080/00222937200770041Google Scholar
Fabricius, O (1780) Fauna Groenlandica, Systematice Sistens Animalia Groenlandiae occidentalis Hactenus indagata, Quoad Nomen Specificum, triviale, Vernaculumque; Synonyma Auctorum Plurium, Descriptionem, Locum, victum, Generationem, Mores, Usum, Capturamque Singuli, Prout Detegendi Occasio Fuit, Maximaque Parte secundum Proprias Observationes. Copenhagen: Ioannis Gottlob Rothe.Google Scholar
Franzén, Å (1977) Gametogenesis of bryozoans. In Woollacott, RM and Zimmer, RL (eds), Biology of Bryozoans. New York, NY: Academic Press, pp. 1–22.Google Scholar
Friedl, H (1925) Kolonienbildung. Besiedelung und Wachstum bei marinen Bryozoen. Arbeiten aus der Zoologischen Institut der Universität Innsbruck 2, 139–168.Google Scholar
Gautier, YV (1962) Recherches écologiques sur les Bryozoaires Chilostomes en Méditerranèe Occidentale. Recueil des Travaux de la Stations Marine d'Endoume 39, 1–434.Google Scholar
Gordon, DP (1970) Reproductive ecology of some northern New Zealand Bryozoa. Cahiers de Biologie Marine 11, 307–323.Google Scholar
Gordon, DP (1977) The aging process in bryozoans. In Woollacott, RM and Zimmer, RL (eds), Biology of Bryozoans. New York, NY: Academic Press, pp. 335–376.10.1016/B978-0-12-763150-9.50016-7Google Scholar
Gostilovskaya, MG (1978) Identification Keys of the White Sea Bryozoans. Leningrad: Nauka [in Russian].Google Scholar
Grave, BH (1930) The natural history of Bugula flabellata at Woods Hole, Massachusetts, including the behavior and attachment of the larva. Journal of Morphology 49, 355–383.10.1002/jmor.1050490204Google Scholar
Grave, BH (1933) Rate of growth, age at sexual maturity, and duration of life of certain sessile organisms, at Woods Hole, Massachusetts. Biological Bulletin 65, 375–386.10.2307/1537211Google Scholar
Grishankov, AV, Ninburg, EA and Shkljarevitch, GA (2000) Macrozoobenthos of the Kandalaksha Sanctuary. Flora and Fauna of Sanctuaries 83, 1–72 [in Russian].Google Scholar
Håkkanson, E and Winston, JE (1985) Interstitial bryozoans: unexpected life forms in a high energy environment. In Larwood, GP and Nielsen, C (eds), Recent and Fossil Bryozoa. Fredensborg: Olsen & Olsen, pp. 125–134.Google Scholar
Harvell, CD and Grosberg, RK (1988) The timing in sexual maturity in clonal animals. Ecology 69, 1855–1864.Google Scholar
Hayward, PJ and Ryland, JS (1975) Growth, reproduction and larval dispersal in Alcyonidium hirsutum (Fleming) and some other Bryozoa. Pubblicazioni della Stazione Zoologica di Napoli 39(suppl.), 226–241.Google Scholar
Herrera, A, Jackson, JBC, Hughes, DJ, Jara, J and Ramose, H (1996) Life-history variation in three coexisting cheilostome bryozoan species of the genus Stylopoma in Panama. Marine Biology 126, 461–469.10.1007/BF00354628Google Scholar
Hughes, DJ (1987) Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina. Journal of Zoology 212, 691–711.10.1111/j.1469-7998.1987.tb05965.xGoogle Scholar
Hughes, DJ (1989 a) Variation in reproductive strategy among clones of the bryozoan Celleporella hyalina. Ecological Monographs 59, 387–403.10.2307/1943073Google Scholar
Hughes, RN (1989 b) Functional Biology of Clonal Animals. London: Chapman & Hall.Google Scholar
Hughes, RN (2005) Lessons in modularity: the evolutionary ecology of colonial invertebrates. Scientia Marina 69, 169–179.10.3989/scimar.2005.69s1169Google Scholar
Hughes, RN, Manríquez, PH, Bishop, JDD and Burrows, MT (2003) Stress promotes maleness in hermaphroditic modular animals. Proceedings of the National Academy of Sciences USA 100, 10326–10330.10.1073/pnas.1334011100Google Scholar
Hyman, LH (1959) The Invertebrates: Smaller Coelomate Groups. Vol. 5: VIII. New York, NY: McGraw-Hill.Google Scholar
Iliash, LV, Zhitina, LS and Fedorov, VD (2003) Phytoplankton of the White Sea. Moscow: Janus-K [in Russian].Google Scholar
Jackson, JBC (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. American Naturalist 3, 743–767.10.1086/283203Google Scholar
Jackson, JBC and Coates, AG (1986) Life cycles and evolution of clonal (modular) animals. Philosophical Transactions of the Royal Society B 313, 7–22.10.1098/rstb.1986.0022Google Scholar
Jackson, JBC and Wertheimer, SP (1985) Patterns of reproduction in five common species of Jamaican reef-associated bryozoans. In Nielsen, C and Larwood, GP (eds), Bryozoa: Ordovician to Recent. Fredensborg: Olsen & Olsen, pp. 161–168.Google Scholar
Jenkins, HL, Bishop, JDD and Hughes, RN (2015) Prudent female allocation by modular hermaphrodites: female investment is promoted by the opportunity to outcross in cyclostome bryozoans. Biological Journal of the Linnean Society 116, 593–602.Google Scholar
Khlebovitch, VV (1974) Critical Salinity of Biological Processes. Leningrad: Nauka [in Russian].Google Scholar
Kluge, GA (1975) Bryozoa of the Northern Seas of the USSR. Keys on the Fauna of the USSR Published by the Zoological Institute, Academy of Sciences of the USSR 76, 1–711. New Delhi: Amerind Publishing.Google Scholar
Kuklinski, P, Berge, J, McFadden, L, Dmoch, K, Zajaczkowski, M, Nygård, H, Piwosz, K and Tatarek, A (2013 a) Seasonality of occurrence and recruitment of Arctic marine benthic invertebrate larvae in relation to environmental variables. Polar Biology 36, 549–560.Google Scholar
Kuklinski, P, Sokolowski, A, Ziolkowska, M, Balazy, P, Novosel, M and Barnes, DK (2013 b) Growth rate of selected sheet-encrusting bryozoan colonies along a latitudinal transect: preliminary results. In Ernst, A, Schäfer, P & Scholz, J (eds), Bryozoan Studies 2010. Lecture Notes in Earth System Sciences. Vol. 143. Berlin, Heidelberg: Springer, pp. 155–167.Google Scholar
Kuznetzov, VV (1941) Dynamics of the biocenosis of Microporella ciliata in the Barents Sea. Proceedings of the Zoological Institute of the Academy of Sciences of USSR 7, 114–139 [in Russian with French summary].Google Scholar
Legendre, P and Legendre, LF (2012). Numerical ecology. 3rd edn. Developments in Environmental Modelling. Vol. 24. Amsterdam, Oxford: Elsevier, pp. i–xvi, 1–990.Google Scholar
Lutaud, G (1985) Preliminary experiments on interzooidal metabolic transfer in anascan bryozoans. In Nielsen, C and Larwood, GP (eds), Bryozoa: Ordovician to Recent. Fredensborg: Olsen & Olsen, pp. 183–191.Google Scholar
Makarov, VN and Shoshina, EV (1996) Dynamics of seasonal growth of Laminaria saccharina in the Barents Sea. Biologija Morja 4, 238–248 [in Russian].Google Scholar
Marcus, E (1926) Bryozoa. In Grimpe, G and Wagler, E (eds), Die Tierwelt der Nord und Ostsee. Vol. 4 (7c). Leipzig: AVG, pp. 1–100.Google Scholar
Mawatari, S (1951) The natural history of a common fouling bryozoan, Bugula neritina (Linnaeus). Miscellaneous Reports of the Research Institute for Natural Resources of Tokyo 20, 47–54.Google Scholar
McKinney, FK and Jackson, JDC (1989) Bryozoan Evolution. Boston, MA: Unwin Hyman.Google Scholar
Médioni, A (1972) Les peuplements sessile des fonds rocheux de la region de Banyuls-sur-Mer: Ascidies-Bryozoaires (Premiere partie). Vie et Milieu B 21, 591–656.Google Scholar
Mukai, H, Terakado, K and Reed, CG (1997) Bryozoa. In Harrison, FW (ed.), Microscopic Anatomy of Invertebrates. Vol. 13. New York, NY: Wiley-Liss, pp. 45–206.Google Scholar
Nekliudova, UA, Schwaha, T, Kotenko, ON, Gruber, D, Cyran, N and Ostrovsky, AN (2019) Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea. Journal of Morphology 280, 278–299.Google Scholar
Nielsen, C (1981) On morphology and reproduction of Hippodiplosia insculpta and Fenestrulina malusii (Bryozoa, Cheilostomata). Ophelia 20, 91–125.Google Scholar
Nielsen, C (1990) Bryozoa Ectoprocta. In Adiyodi, KG and Adiyodi, RG (eds), Reproductive Biology of Invertebrates. Vol. 4, Part B: Fertilization, Development, and Parental Care. New Delhi: IBH Publishing, pp. 185–200.Google Scholar
Nielsen, C (2013) Bryozoa (Ectoprocta: ‘Moss’ animals). In eLS. Chichester: Wiley, pp. 1–6.Google Scholar
O'Dea, A (2006) Asexual propagation in the marine bryozoan Cupuladria exfragminis. Journal of Experimental Marine Biology and Ecology 335, 312–322.Google Scholar
O'Dea, A, Jackson, JBC, Taylor, PD and Rodríguez, F (2008) Modes of reproduction in recent and fossil cupuladriid bryozoans. Palaeontology 51, 847–864.Google Scholar
O'Dea, A, Ostrovsky, AN and Rodrígues, F (2010) Embryonic brooding and clonal propagation in tropical eastern Pacific cupuladriid bryozoans. Journal of the Marine Biological Association of the United Kingdom 90, 291–299.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O’Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2017) Vegan: Community Ecology Package. R package version 2.4-4. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Orton, JH (1914) Preliminary account of a contribution to an evaluation of the sea. Journal of the Marine Biological Association of the United Kingdom 10, 312–326.Google Scholar
Ostrovsky, AN (1998) Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida). Acta Zoologica 79, 287–318.Google Scholar
Ostrovsky, AN (2013) Evolution of Sexual Reproduction in Marine Invertebrates: Example of Gymnolaemate Bryozoa. Dordrecht: Springer Verlag.Google Scholar
Pace, RM (1906) On the early stages in the development of Flustrellidra hispida (Fabricius), and on the existence of a “yolk nucleus” in the egg of this form. Quarterly Journal of Microscopical Science 50, 435–478.Google Scholar
Powell, NA (1967) Sexual dwarfism in Cribrilina annulata (Cribrilinidae-Bryozoa). Journal of the Fisheries Research Board of Canada 24, 1905–1910.Google Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna: R Foundation. Available at https://www.R-project.org/.Google Scholar
Reed, CG (1987) Bryozoa. In Strathmann, MF (ed.) Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast: Data and Methods for the Study of Eggs, Embryos, and Larvae. Seattle: University of Washington Press, pp. 494–510.Google Scholar
Reed, CG (1988) The reproductive biology of the gymnolaemate bryozoan Bowerbankia gracilis (Ctenostomata: Vesiculariidae). Ophelia 29, 1–23.10.1080/00785326.1988.10430816Google Scholar
Reed, CG (1991) Bryozoa. In Giese, AC, Pearse, JS and Pearse, VB (eds), Reproduction of Marine Invertebrates. Vol. 6: Echinoderms and Lophophorates. Pacific Grove, CA: Boxwood Press, pp. 85–245.Google Scholar
Ryland, JS (1963) Systematic and biological studies on Polyzoa (Bryozoa) from western Norway. Sarsia 14, 1–59.Google Scholar
Ryland, JS (1967) Polyzoa. Oceanography and Marine Biology 5, 343–369.Google Scholar
Ryland, JS (1970) Bryozoans. London: Hutchinson University Library.Google Scholar
Ryland, JS (1976) Physiology and ecology of marine bryozoans. In Russell, FS and Yonge, CM (eds), Advances in Marine Biology. Vol. 14. London, New York: Academic Press, pp. 285–443.Google Scholar
Ryland, JS (1979) Structural and physiological aspects of coloniality in Bryozoa. In Larwood, GP and Rosen, BR (eds), Biology and Systematics of Colonial Organisms. Systematics Association special vol. 11. London: Academic Press, pp. 211–242.Google Scholar
Ryland, JS (2005) Bryozoa: An introductory overview. In Woess, E (ed.) Moostiere (Bryozoa). Denisia. Vol. 16. Linz: Biologiezentrum des Oberösterreichischen Landesmuseums, pp. 9–20.Google Scholar
Seed, R and Hughes, RN (1992) Reproductive strategies of epialgal bryozoans. Invertebrate Reproduction and Development 22, 291–300.Google Scholar
Shoshina, EV (1998) Red algae. In Commercial and Perspective for Use Algae and Invertebrates of the Barents and White Seas. Apatity: KNC RAN, pp. 187–212 [in Russian].Google Scholar
Shunkina, KV (2008) Geographic and Biotopic Variability in Size of Bryozoan Cribrilina annulata (Fabricius, 1780) on different Stages of Life Cycle (BSc Thesis). Saint Petersburg State University, Saint Petersburg, Russia [in Russian].Google Scholar
Shunkina, KV (2010). Reconstruction of the Life-Cycle of Cheilostome Bryozoan Cribrilina annulata (Bryozoa: Gymnolaemata) on the Laminarian Thalli (White Sea, Chupa Inlet) (MSc Thesis). Saint Petersburg State University, Saint Petersburg, Russia [in Russian].Google Scholar
Shunkina, KV and Yagunova, EB (2008) Geographic and biotopic size variability in the bryozoan Cribrilina annulata (Fabricius, 1780) on the different stages of the life-cycle. In Materials of the Scientific Conference Devoted to the 70 th Anniversary of the White Sea Biological Station Named after N.A. Pertsov. Moscow: Grif & Co., pp. 143–146 [in Russian].Google Scholar
Silén, L (1945) The main features of the development of the ovum, embryo and ooecium in the ooecioferous Bryozoa Gymnolaemata. Arkiv för Zoologi 35A, 1–34.Google Scholar
Sokolover, N, Ostrovsky, AN and Ilan, M (2018) Schizoporella errata (Bryozoa: Cheilostomata) in the Israeli Mediterranean Sea: abundance, growth rate and reproduction strategy. Marine Biology Research 14, 868–882.Google Scholar
Soule, JD and Soule, DF (1977) Fouling and bioadhesion: life strategies of bryozoans. In Woollacott, RM and Zimmer, RL (eds), Biology of Bryozoans. New York, NY: Academic Press, pp. 437–457.Google Scholar
Stearns, CS (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87, 476–486.Google Scholar
Stebbing, ARD (1972) Preferential settlement of a bryozoan and serpulid larvae on the younger parts of Laminaria fronds. Journal of the Marine Biological Association of the United Kingdom 52, 765–772.Google Scholar
Taylor, PD (1999) Bryozoans. In Savazzi, E (ed.), Functional Morphology of the Invertebrate Skeleton. Chichester: John Wiley & Sons, pp. 623–646.Google Scholar
Taylor, PD (2005) Bryozoans. In Taylor, PD and Lewis, DN (eds), Fossil Invertebrates. London: Natural History Museum, pp. 310–320.Google Scholar
Todd, CD (1998) Larval supply and recruitment of benthic invertebrates: do larvae always disperse as much as we believe? Hydrobiologia 375/376, 1–21.Google Scholar
Vozzhinskaya, VB (1977) Biology (Seasonal Development and Productivity) of Laminaria of the White Sea. Moscow: Pischcevaya Promyshlennost [in Russian].Google Scholar
Williams, GA and Seed, R (1992) Interactions between macrofaunal epiphytes and their host algae. In Hawkins, SJ, John, DM and Price, JH (eds), Plant-Animal Interactions in the Marine Benthos. Systematics Association special vol. 46. London: Academic Press, pp. 189–211.Google Scholar
Winston, JE (1983) Patterns of growth, reproduction and mortality in bryozoans from the Ross Sea, Antarctica. Bulletin of Marine Science 33, 688–702.Google Scholar
Winston, JE and Håkkanson, E (1986) The interstitial bryozoan fauna from Capron Shoal, Florida. American Museum Novitates 2865, 1–50.Google Scholar
Wood, V and Seed, R (1992) Reproduction and growth of Alcyonidium hirsutum (Fleming) and Flustrellidra hispida (Fabricius) (Bryozoa: Ctenostomata) within a Fucus serratus community. Cahiers de Biologie Marine 33, 347–363.Google Scholar
Woollacott, RM (1999) Bryozoa (Ectoprocta). In Knobil, E and Neill, JD (eds), Encyclopedia of Reproduction. Vol. 1. New York, NY: Academic Press, pp. 439–448.Google Scholar
Yagunova, EB (2005 a) Astogeny of Cribrilina annulata (Fabricius, 1780) (Bryozoa, Cheilostomata): norm and anomaly. Invertebrate Zoology 2, 36–50 [in Russian].Google Scholar
Yagunova, EB (2005 b) Geographic and biotopic variability of zooidal size in Cribrilina annulata (Bryozoa, Cheilostomata). Vestnik Sankt-Petersburgskogo Universiteta, Biologia 3, 17–25 [in Russian].Google Scholar
Yagunova, EB and Ostrovsky, AN (2008) Encrusting bryozoan colonies on stones and algae: variability of zooidal size and its possible causes. Journal of the Marine Biological Association of the United Kingdom 88, 901–908.Google Scholar
Yagunova, EB and Ostrovsky, AN (2010) The influence of substrate type on sexual reproduction of the bryozoan Cribrilina annulata (Gymnolaemata, Cheilostomata): a case study from Arctic seas. Marine Biology Research 6, 263–270.Google Scholar
Yoshioka, PM (1973) The Population Dynamics and Ecology of the Encrusting Ectoproct Membranipora serrilamella (PhD Dissertation). University of California, San Diego, California.Google Scholar
Yoshioka, PM (1982) Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology 63, 457–468.Google Scholar
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