Australian BRYOZOA Volume 1 Biology, Ecology and Natural History Editors: Patricia L. Cook, Philip E. Bock, Dennis P. Gordon and Haylee J. Weaver Australian BryozoA Volume 1 Biology, Ecology and Natural History Editors: Patricia L. Cook, Philip E. Bock, Dennis P. Gordon and Haylee J. Weaver © Commonwealth of Australia 2018 All rights reserved. Except under the conditions described in the Australian Copyright Act 1968 and subsequent amendments, no part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, duplicating or otherwise, without the prior permission of the copyright owner. Contact CSIRO Publishing for all permission requests. A catalogue record for this book is available from the National Library of Australia. Published by CSIRO Publishing Locked Bag 10 Clayton South VIC 3169 Australia Telephone: +61 3 9545 8400 Email: [email protected] Website: www.publish.csiro.au Front cover: Celleporaria spp. on a wharf pile (photo: K. Gowlett-Holmes) Set in 10.5/14 Palatino and Optima Edited by Peter Storer Cover design by James Kelly Typeset by Thomson Digital Index by Max McMaster Printed in China by 1010 Printing International Ltd Series editor: H.J. Weaver Series graphics design: B. Kuchlmayr Volume 1 to be cited as: Cook PL, Bock PE, Gordon DP and Weaver HJ (eds) (2018) Australian Bryozoa Volume 1: Biology, Ecology and Natural History. CSIRO Publishing, Melbourne. Individual chapters cited as: Bock PE, Cook PL and Gordon DP (2018) General morphology and terminology. In Cook PL, Bock PE, Gordon DP and Weaver HJ (eds) Australian Bryozoa Volume 1: Biology, Ecology and Natural History. pp. xx–xx. CSIRO Publishing, Melbourne. 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Contents List of authors v 1 Introducing bryozoans 1 Patricia L. Cook, Dennis P. Gordon, Peter J. Hayward, Philip E. Bock and Yvonne Bone 1.1 Introduction 1 1.2 Phylogeny and classification 2 1.3 Ecology of bryozoans 5 1.4 Economic significance 10 References 11 2 History of discovery in Australian waters 17 Philip E. Bock, Patricia L. Cook and Dennis P. Gordon 2.1 Introduction 17 2.2 Early collections: 1700s and 1800s 17 2.3 Collecting in the 1900s 21 2.4 Bryozoa to the present, and current status of collecting 22 References 23 3 General morphology and terminology 29 Philip E. Bock, Patricia L. Cook and Dennis P. Gordon 3.1 External characteristics and astogeny 29 3.2 Skeletal system 31 3.3 Colonial tropisms, kineses and mobility 33 3.4 Feeding and digestive system 34 3.5 Interzooidal communications and the funicular system 36 3.6 Respiration and excretion 38 3.7 Degeneration and regeneration cycles 38 3.8 Nervous system and sense organs 39 3.9 Glandular systems 40 3.10 Reproduction 40 3.11 Genetic studies 45 References 47 4 Modern and Cenozoic bryozoan colony classification schemes 55 Yvonne Bone 4.1 Introduction 55 4.2 Examples of bryozoan growth forms 56 4.3 Substratum and attachment 61 4.4 Conclusion 62 Acknowledgements 63 References 63 5 Bryozoans on seamounts 65 Dennis P. Gordon 5.1 Introduction 65 5.2 Australian seamounts 65 5.3 Bryozoans on Australian and New Zealand seamounts 66 References 68 iv AustrAliAn BryozoA 6 Bryozoans and biosecurity 71 Dennis P. Gordon 6.1 Introduction 71 6.2 Bryozoans as marine-fouling organisms 71 6.3 Alien bryozoans in Australia 73 6.4 Conclusion 84 References 84 Colour plates 91 7 Bryozoans and biotechnology 121 Michèle Prinsep 7.1 Introduction 121 7.2 Compounds isolated from bryozoans 122 7.3 Compounds used against bryozoans 131 7.4 Conclusion 132 References 132 8 Bryozoans and ocean acidification 139 Abigail M. Smith 8.1 Ocean acidification: an old, but new global problem 139 8.2 What can we do about acidification? 140 8.3 Bryozoans as potential allies 140 8.4 Bryozoans as ‘canaries’ 140 8.5 Bryozoan growth models 141 8.6 Bryozoans as sentinels 142 8.7 Conclusion 142 References 143 9 Bryozoans in the marine benthos 145 Robyn L. Cumming, Dennis P. Gordon and Karen Gowlett-Holmes 9.1 Introduction 145 9.2 Temperate benthic environments 146 9.3. Tropical benthic environments 150 9.4. Environmental correlates 156 9.5. Bryozoans as habitat 157 Acknowledgements 157 References 158 10 Fossil bryozoans of Australia section A – Palaeozoic era 163 Catherine M. Reid A10.1 Introduction 163 A10.2 Class Stenolaemata (range Ordovician to Recent) 163 A10.3 Class Gymnolaemata (range Ordovician to Recent) 164 section B – Mesozoic–Cenozoic eras 165 Rolf Schmidt B10.1 Mesozoic 165 B10.2 Cenozoic 165 References 167 Glossary 171 Index 177 LIst oF A utHors Philip E. Bock Peter J. Hayward Museum Victoria, Melbourne, Victoria 3001, School of Biological Sciences, University of Wales, Australia Swansea, United Kingdom Yvonne Bone Michèle Prinsep School of Earth and Environmental Sciences, Uni- School of Science, University of Waikato, Hamilton versity of Adelaide, Adelaide, South Australia 5005, 3240, New Zealand Australia Catherine M. Reid Patricia L. Cook (deceased) Department of Geological Sciences, University of Glen Waverley, Victoria 3150, Australia Canterbury, Christchurch 8140, New Zealand Robyn L. Cumming Rolf Schmidt Museum of Tropical Queensland, Townsville, Museum Victoria, Melbourne, Victoria 3001, Queensland 4810, Australia Australia Dennis P. Gordon Abigail M. Smith National Institute of Water and Atmospheric Department of Marine Science, University of Otago, Research, Wellington 6021, New Zealand Dunedin 9054, New Zealand Karen Gowlett-Holmes CSIRO Marine Laboratories, Hobart, Tasmania 7000, Australia This page intentionally left blank 1 Introducing bryozoans Patricia L. Cook, Dennis P. Gordon, Peter J. Hayward, Philip E. Bock and Yvonne Bone 1.1 Introduction growth, some living species in shallow coastal water or on the present-day continental shelf form Bryozoans are aquatic animals that form colonies important seafloor habitat for a variety of other of connected individuals. Bryozoans have such highly variable morphology that they are often organisms including economically important fish mistaken for other organisms such as hydroids, and shellfish. Some species have shown promise as corals, colonial ascidians and turfing seaweeds. sources of marine natural products such as anti- Some colonies are bushy and moss-like, hence the cancer, antiviral and antifouling substances. phylum name, Bryozoa, which means ‘moss ani- Bryozoa are aquatic and mostly marine, with mals’ in Greek. Others are flat and encrusting, species found in all oceans from sublittoral to abys- hence the common name ‘sea mats’. Still others sal depths. Freshwater species inhabit high mon- resemble lace, forming erect frondose colonies with tane lakes, and ponds, streams and rivers in all holes in their structure or encrustations over sea- continents except Antarctica. More than 6300 living weeds and rocks, hence the name ‘lace corals’. Since species (WoRMS Editorial Board 2017) and 15 000 no single common name is applicable to all species, fossil species have been described. Including the name ‘bryozoans’ is the one most preferred by known but undescribed species, the Australian researchers of the group. fauna currently stands at around 1200 species: the Bryozoans have long had a reputation for being highest for any country in the world. This figure, a minor, sometimes unimportant phylum, but they however, is highly conservative and it is likely that are by no means rare. In some habitats they are the the Australian fauna includes well over 2000 spe- dominant organisms. Some species foul boat bot- cies. The group has a long fossil history, beginning toms and ship hulls, marinas, pontoons, wharf in the earliest Ordovician; both past and present piles and even reticulation systems of marine and faunas are highly abundant and diverse. freshwater installations. Because they can settle on Each bryozoan colony (sometimes referred to by vessels, some bryozoan species are important alien palaeontologists as the zoarium – the fossil skeletal invasives. Other species can be abundant on some expression of the colony) is a series of clones of tiny parts of the continental shelf and, over geological genetically identical members called zooids, which time, their shelly remains, along with molluscan may be highly varied in size and shape. Each shell and the carbonate remains of other organ- colony begins as a single zooid, the ancestrula, isms, have been fossilised into limestone forma- which forms when a larva settles on substrata and tions that now outcrop on land. With their robust metamorphoses. The ancestrula buds off daughter 2 AustrAliAn BryozoA zooids, which in turn bud additional zooids until known as polymorphs), and their forms and func- the colony reaches its optimum size. Depending on tions vary widely within and between species, species, a mature colony may have only two or genera and families. Heterozooid form is com- three, or many millions of zooids, and as a result monly used to define taxa, at every taxonomic may range in size from less than 1 mm to more level, despite a growing appreciation of the adap- than 1 m. Colonies are usually sessile, developing tive nature of these zooids. Kenozooids are the from a motile larva by settlement and metamor- simplest type of polymorph. Spines, rhizoids (root- phosis, and live attached to a substratum such as lets) and some brooding structures are kenozooids. rock, shell or algae, or wood. They often colonise The term denotes an empty unit – a coelomic cavity other animals, such as hydroids, gorgonians and bounded by a body wall but lacking a tentacle other bryozoans. A few forms have rootlet-like crown and orifice. It may be similar in shape and rhizoids that anchor them directly into the sedi- size to an autozooid, or radically different from it. ment, and others are unattached, living intersti- Size, shape, and function vary continuously among tially in the surface layers. Some unattached species structures defined as kenozooids; homologies are capable of motility: ‘walking’ or lurching by the between these are not always clear, and the devel- aid of bristle-like structures on the colony opmental processes giving rise to them are not periphery. always predictable. Most bryozoans have a calcareous skeleton, except for the members of the freshwater class Phy- 1.2 Phylogeny and classification lactolaemata and the mostly marine Ctenostomata (class Gymnolaemata), which have non-calcified Bryozoans have certainly been known to European colonies. Colonies are hermaphrodite, although naturalists for more than 450 years (Wyse Jackson individual zooids may contain either ovaries or and Spencer Jones 2002), yet, interestingly, the testes, or both, or neither. All bryozoans are sus- wider relationships of the phylum are as puzzling pension feeders, capturing small living and non- in the 21st century as they were in the 18th century living particles from water. Accordingly, most (see Box 1.1). Although there is emerging consen- zooids in a colony are feeding zooids, called auto- sus based on gene sequencing and molecular data, zooids. Each autozooid has an eversible bell-shaped controversy still remains. The animal nature of cluster of ciliated tentacles (the tentacle crown) bryozoans was suggested by Peyssonnel (Watson that entrap food particles. The mouth is situated at 1751–52; Peyssonnel 1756) and others, but was not the base of the circlet of tentacles and leads to a generally accepted until the publication of the Nat- U-shaped digestive tract; the anus opens exterior to ural History of the Corallines by Ellis in 1755. Lin- the base of the tentacle crown (Plate 1.1). The organs naeus (1758) included them with coelenterates in and tissues in an autozooid that undergo periodic Zoophyta (‘animal-plants’), considering them to be replacement – namely, tentacles, tentacle sheath, partly of a plant nature. The discovery that bryozo- alimentary canal, associated musculature and ans had a tubular gut, with a mouth and anus, as nerve ganglion – are collectively termed a polypide well as ciliated tentacles, eventually led to their (Hayward and Ryland 1979). separation from coelenterates as Polyzoa (‘many The colonies of many species are highly poly- animals’) by Thompson (1830) and Bryozoa (‘moss morphic (meaning ‘many forms’), having a variety animals’) by Ehrenberg (1831) (see Box 1.2). Milne of non-feeding zooids that exhibit a range of form Edwards (1843) grouped bryozoans with molluscs and function. These other types of zooids may sup- and tunicates as Molluscoidea – an assemblage to port the autozooids, or be budded in distinctive which brachiopods were later added – and this patterns on or among them. Collectively, all poly- concept, in part at least, extended into the 20th morphic zooids are termed heterozooids (also century. 1 – IntroducIng bryozoans 3 Box 1.1. Bryozoa by another name Historically, bryozoans were confused with other organisms and, owing to the plant-like appearance of some, were considered among the ‘zoophytes’ (literally ‘animal-plants’) of the early naturalists. Other phylum names have been applied to Bryozoa. For example, Polyzoa (‘many animals’, referring to the colonies of a few to millions of individuals) was once commonly used in Britain and Australasia. The name was introduced by the English naturalist J.V. Thompson in 1830 – a year earlier than German scientist Gottfried Ehrenberg (1831) introduced Bryozoa – but rules of nomenclatural priority do not apply to higher taxa. Ectoprocta (which alludes to the fact that the anus opens outside the ring of tentacles, in contradistinction to Entoprocta) and Entoprocta were introduced as subdivisions of Bryozoa by Heinrich Nitsche in 1869. Each was elevated to a phylum by Hatschek (1888). Europeans and North Americans have traditionally used the name Bryozoa and this was the name formally accepted by the International Bryozoology Association when the association was inaugurated in 1965 (Cheetham 2002). Unfortunately, the late Libbie Hyman (1959), author of a highly authoritative series of books on the invertebrates, resurrected the name Ectoprocta. Since Hyman’s work, some influential textbooks in the United States resulted in the perpetuation of this name, which has now been superseded in favour of Bryozoa (Nielsen 2012; Ruggiero et al. 2015). Box 1.2. Place in the animal kingdom Bryozoans are protostomes (Greek, protos, first, stoma, mouth). Technically, a protostome is an animal in which the first opening in the embryo becomes the mouth – present in flatworms, molluscs, annelids and arthropods. However, this feature can be equivocal in bryozoans, owing to the particular mode of embryonic development. Currently, as indicated by nucleic acid sequencing, as well as some anatomical and embryological studies, bryozoans are classified among the Lophotrochozoa (Spiralia), that sub-branch of the Protostomia that includes segmented worms, molluscs, brachiopods and their kin, to the exclusion of the moulting animals (Ecdysozoa): that is, insects, crustaceans and other arthropods, plus nematode worms and related small phyla. The precise relationships of Bryozoa within the Lophotrochozoa are still unclear, however. Several molecular studies have segregated them from Brachiopoda (lamp shells) and Phoronida (horseshoe worms), with which they had earlier been grouped based on several morphological criteria, and allied them instead with Entoprocta and Cycliophora. Nesnidal et al. (2013) have recovered a Lophophorata clade that re-unites bryozoans with the other ‘lophophorate’ groups based on molecular criteria, but, as Nielsen (2012) has pointed out, whereas Brachiopoda and Phoronida have monociliated epithelial cells, those of Bryozoa are multiciliated. This is a non-trivial distinction and the question of close relationship remains open. This history of nomenclature nevertheless gives pointed out that, whereas brachiopods and phoro- an indication of the various other phyla to which nids have monociliated epidermal cells, bryozoans bryozoans have been deemed to be related on mor- have multiciliated epidermal cells – a phylogeneti- phological grounds. One persuasive arrangement cally significant feature. Moreover, the mode of has been that of Lophophorata (Hatschek 1888; beating of ciliary tracts for suspension feeding is Hyman 1959), uniting Bryozoa, Brachiopoda and downstream-collecting in Bryozoa and upstream- Phoronida on the basis of a structurally similar collecting in Brachiopoda and Phoronida. These, feeding apparatus (the tentacle crown) deemed to and other embryological characteristics, united bra- be homologous, along with a perceived tripartite chiopods and phoronids with core deuterostomes body plan. In his comprehensive morphological (echinoderms, hemichordates, tunicates and chor- analysis of the animal kingdom, Nielsen (1995) dates) and allied bryozoans with Entoprocta in