Colonial integration and the maintenance of colony form in encrusting bryozoans Elisa K. Bone Thesis submitted in total fulfilment of the requirements for the degree of Doctor of Philosophy November 2006 Department of Zoology The University of Melbourne Abstract The form of an organism is often closely linked to its function, and this relationship may be particularly important in organisms where individual form is highly flexible due to the repeated iteration of minute multicellular modules. In many modular taxa, including the bryozoans discussed in this thesis, each module is able to function as largely independent units; an individual module can feed independently, has a separate gut, and has the potential to reproduce. These characteristics mean that the number of modules in a bryozoan colony, and hence its size, is a reasonably accurate measure of the colony’s ability to both capture resources and to produce sexually developed larvae. Size is therefore a more appropriate measure of colony demography than age, the criterion traditionally used for unitary organisms. However, processes that can complicate the demography of modular organisms such as colony damage, fission or fusion also mean that the age structure of the component modules in a colony or fragment remains an important predictor of colony functioning, interacting with the effects of colony size. Effective colony functioning in a sessile invertebrate necessitates a level of coordination between component zooids; enabling a colony to grow, reproduce, to compete with neighbouring organisms and, in some cases, to develop defensive structures in response to predation threats. In cheilostome bryozoan colonies, individual zooids are extremely compartmentalised, and connections are reduced to tiny pores that enable the transport of nutrients between zooids within a colony. Component zooids may also differ in size, shape and function across colony regions, subsequently affecting their energy requirements and their capacity to both capture resources and transmit nutritious foodstuff to other members of the colony. Changes in colony size through normal growth may also lead to changes in the energy requirements and resource capture rates of individual zooids, since zooid age interacts with the colony’s patterns of module addition and expansion to determine the capacity for growth, reproduction and other functions within an undamaged colony. In Watersipora subtorquata, a common unilaminar cheilostome bryozoan species with very low levels of polymorphism and a regular budding pattern, zooid measurements varied over the course of colony development, and i feeding rates in colonies of differing sizes indicated that smaller colonies may have higher energy requirements than larger colonies. In addition, over hour-long feeding trials, not all zooids were feeding at any one time. Since the provision of resources to the undeveloped, non-feeding zooids at the edge must be by other feeding zooids in the colony, some transport of resources must be taking place between zooids to meet the colony’s energy requirements. I examined internal measures of the capacity for inter-zooid resource transfer in 5 species of encrusting bryozoan using scanning electron microscopy (SEM) to visualise the communication pores within the funicular system, and quantified variation in these pores across colony regions in three species. In Watersipora subtorquata and Conopeum seurati, the patterns of pores indicated that resource transfer is strongly directed towards the (growing) colony edge, and this finding correlates well with observations of rapid growth in the field. In the third species, Mucropetraliella ellerii, directional transfer towards the edge appeared weaker, and may be due to the damage history, reproductive state or age of the colony fragments. This result could also be indicative of a lower capacity for growth at the colony edge. Further detailed examination of the communication pores and their formation suggested that the funicular system may be quite flexible in cheilostome bryozoans, and that existing pores may be closed or opened, or the direction of transfer altered, through the formation of new porous connections. Another indicator of the level of integration within a colony is the way a colony responds to external stressors such as the removal of zooids or the close proximity of other organisms. I examined the capacity for recovery in Watersipora subtorquata colonies both after repeated removal of the growing edge and after the removal of groups of zooids from different colony regions in colonies that varied in size, with the explicit aim to assess the potential for nutritious resources to be re-directed after the disruption of colony form. Where the growing edge was removed, colonies showed large decreases in total growth and reproduction compared to undamaged colonies. However, there was some indication that resources may be re-directed towards the colony centre, with the rate of zooid death in the centre of damaged colonies lower than the rate seen in undamaged colonies. Similarly, where colonies were damaged in different colony regions, colony ii size appeared to interact with the type of damage, and some regeneration contrary to the primary direction of growth was seen in larger colonies. Where colonies that are genetically similar or otherwise compatible are growing in close proximity, fusion to form a single colony may be a viable response, increasing a colony’s size, which in turn improves its competitive abilities and reproductive capacity. In these cases, we might expect compatible colonies in close proximity to show directional growth towards each other, and incompatible colonies to grow in a way that avoids contact. I did not see any discernable effect on growth direction in W. subtorquata colonies that differed in either their level of apparent relatedness or their size, but stronger effects may have been seen with improved sample sizes and longer experimental periods. The importance of the growing edge as a resource sink in encrusting bryozoans appears consistent across taxa, but examination of responses to damage in Parasmittina delicatula under field conditions at two locations showed that local conditions and competition can also affect colony recovery, and in this case were more important than the levels of internal colonial integration. This result highlights the importance of considering possible effects of local conditions in detailed examinations of growth and recovery potential across multiple species in modular organisms. iii Declaration This is to certify that: (i) the thesis comprises only my original work towards the PhD except where otherwise acknowledged (ii) the thesis is less than 100,000 word in length, exclusive of tables, maps, bibliographies and appendices Elisa Bone November 2006 iv Acknowledgments It’s fair to say that almost everybody I have dealt with over the past few years has contributed in some way to this project. The “brians” have become a big part of my life over these years, and the story of their structure and function has been scribbled on countless scraps of paper and serviettes to be explained to anyone that cared to listen. Thank you to you all. ***** More specifically, I thank my supervisor, Mick Keough, who has shown faith in me throughout, and provided support, encouragement, discussions, advice and the voice of reason. To all the members of the Keough lab, past and present – there are too many of you to mention here, but you know who you are – thank you also for your support, friendship, discussions and help over the years. Thank you to those who helped me with field work – Claire Bennett, Nathan Knott, Allyson O’Brien, Matt Reardon, David Reid, and to Bec Loughman for reading drafts. I am very grateful to Joan Clark for teaching me how to use the electron microscope, and then allowing me to use it for hours on end without supervision. Thanks also to Bruce Abaloz for some histology work that provided interesting insights into bryozoan-kelp interactions. Thanks to everybody in the Department of Zoology, especially my fellow post-graduates, to those who helped find suitable microscopes and equipment for my work, and to Garry Jolly-Rogers, David Macmillan, Mark Padgham and Matt Symonds for interesting discussions that helped to refine my research questions. A PORES grant from the Melbourne Scholarships Office and a research grant from the Department of Zoology enabled me to travel to the U.S., and many people helped me in securing and completing my exchange at the University of California, Santa Cruz. Thanks to Pete Raimondi, for agreeing to host me in his lab, to Kathleen Donahue for helping organise my visa requirements, and to Betsy Steele for getting me set up in the lab and helping me find suitable equipment. Huge thanks are due to Todd Newberry and Kerstin Wasson, for insightful discussions and encouragement, and for helping me remember that obscure organisms do not necessarily mean obscure questions. Thanks also to Anna, Becky, Hilary and the guys at Segre – Arnold, Jan and Joni. Finally, many thanks to my friends and family and to my partner, Dave, for everything. v Table of Contents 1. General Introduction................................................................................................... 1 2. Colony form and scaling in Watersipora subtorquata................................................. 9 1. Scaling of zooid size and resource partitioning.....................................................................13