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Sponges As Sensitive Animals: Sensory Systems and Energetics of Filtration in Demosponges

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Sponges As Sensitive Animals: Sensory Systems and Energetics of Filtration in Demosponges Sponges as sensitive animals: sensory systems and energetics of filtration in demosponges by Danielle Alexandra Ludeman A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science In Ecology Department of Biological Sciences University of Alberta © Danielle Alexandra Ludeman, 2015 Abstract Sponges (Porifera) are abundant in most marine and freshwater ecosystems, and as suspension feeders they play a crucial role in filtering the water column. Their active pumping enables them to filter up to 900 times their body volume of water per hour, recycling nutrients and coupling the benthic and pelagic communities. Despite the ecological importance of sponge filter feeding, little is known about how sponges control the water flow through their canal system or how much energy it costs to filter the water. Sponges lack conventional muscles and nervous tissue, yet respond to stimuli through coordinated behaviours. Here, I show the presence of non-motile cilia in the canal system of sponges and study their role as flow sensors. I demonstrate that molecules known to block cationic channels in sensory cilia in other organisms reduce or eliminate sponge behaviour. In addition, removal of the cilia using chloral hydrate eliminates sponge contractions, suggesting the cilia are flow sensors and involved in controlling water flow through the canal system. Sponges have long been considered textbook examples of animals that use current-induced flow. I show evidence that suggests some species of demosponge do not use current-induced flow; rather, they respond behaviourally to increased ambient currents by reducing their pumping volume. Using a morphometric model of the canal system, I also show that filter feeding may be more energetically costly than previously thought. Measurements of pumping volume and oxygen removal in five species of demosponges show that pumping rates are variable within and between species, with more oxygen consumed the greater the pumping volume. Together, these data suggest that sponges have a lot of control over the volume of water pumped, which may be an adaptation to reduce the energetic cost of filtration in times of high stress. ii Preface Chapter Two of this thesis has been published as Ludeman, D. A., Farrar, N., Riesgo, A., Paps, J. and Leys, S. P. (2014). Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges. BMC Evolutionary Biology 14. I was responsible for conceiving experiments, performing the experiments, data analysis, and manuscript composition. Farrar, N., Riesgo, A., Paps, J. and Leys, S.P. performed the molecular analysis. Leys S.P. was the supervisory author and was involved with conceiving experiments, electron microscopy, and manuscript composition. Chapter Three forms part of an international collaboration with Dr. Matthew Reidenbach in the Department of Environmental Sciences at the University of Virginia. iii Acknowledgements This thesis would not have been possible without the support from so many people, near and far. First to my supervisor, Dr. Sally Leys, I owe gratitude for all of your encouragement and guidance over the years. You have opened up my eyes to the world of sponges, and supported me at every stage of both my Honors and Masters degrees. To my committee members, Dr. Rich Palmer and Dr. Mark Lewis, thank you for all of your suggestions and advice throughout my degree. Thank you also to Dr. Matthew Reidenbach for letting me join your Panama trip and providing me invaluable guidance on fluid mechanics as well as technical advice along the way. Thanks to Nathan Farrar for all of your hard work with the transcriptome analysis in Chapter Two, and to my other co-authors Dr. Ana Riesgo and Dr. Jordi Paps for providing technical advice and insightful comments on the published manuscript. I also thank Dr. Gitai Yahel for your guidance on data analysis, and Nelson Lauzon for all of your help building and setting up in both Panama and Bamfield as well as your amazing photography skills. In addition, I received technical help from various students, Emma Carroll and Nhu Trieu to whom I am indebted for all of their work on the histological samples used in Chapter Three, and Matt Oldach who helped create the MATLAB scripts in Appendix Two. I have received a great deal of support from other graduate students both in the department and the lab. Thank you to Emily Adams and Pam Windsor for helping me get settled into the lab and passing on their prior sponge knowledge. Amanda Kahn, Rachel Brown, and Christianne McDonald, I am truly grateful for all of the support that you have given me over the years. I know you will always be there, on the good days and the bad, and I look forward to many more laughs in the years to come. Finally, to my wonderful friends and family who have continuously provided encouragement and support throughout the years. And to my husband, Brian Pendlebury, I am forever thankful for your love and encouragement. This work was funded by the Department of Biological Sciences, an NSERC PGSM, Queen Elizabeth II scholarship, Nortek equipment grant, Company of Biologists Travel Fellowship, Bamfield John Boom scholarship, Donald M. Ross scholarship, and an NSERC Discovery Grant to Dr. Sally Leys. iv Table of Contents Chapter One A GENERAL INTRODUCTION TO BEHAVIOUR AND FILTER-FEEDING IN SPONGES _ 1 1.1 Ecology of sponges _______________________________________________________ 1 1.2 Anatomy of sponges ______________________________________________________ 4 1.3 Sponges are sensitive to their environments ____________________________________ 7 1.4 Filter feeding and its energetic cost in sponges _________________________________ 10 1.5 Use of current-induced flow _______________________________________________ 12 1.6 Thesis objectives and outlines ______________________________________________ 15 1.7 References _____________________________________________________________ 16 Chapter Two EVOLUTIONARY ORIGINS OF SENSATION IN METAZOANS: FUNCTIONAL EVIDENCE FOR A NEW SENSORY ORGAN IN SPONGES ________________________ 22 2.1 Introduction ____________________________________________________________ 22 2.2 Methods _______________________________________________________________ 23 2.2.1 Summary of experimental design ________________________________________ 23 2.2.2 Collecting and culturing of sponges ______________________________________ 24 2.2.3 Fixation for fluorescence microscopy ____________________________________ 24 2.2.4 Fixation for scanning and transmission electron microscopy (SEM, TEM) _______ 25 2.2.5 Orientation analysis __________________________________________________ 25 2.2.6 Assessment of the possible sensory role ___________________________________ 25 2.2.7 BioInformatics ______________________________________________________ 27 2.3 Results and Discussion ___________________________________________________ 28 2.3.1 Sponge oscula are ciliated _____________________________________________ 28 2.3.2 Cationic channel blockers inhibit sponge behaviour _________________________ 29 2.3.3 Sponges possess a repertoire of transient receptor potential channels ___________ 38 2.4 Conclusions ____________________________________________________________ 41 2.5 References _____________________________________________________________ 42 Chapter Three IT COSTS MORE TO PUMP MORE: ENERGETIC COST OF FILTRATION AND BEHAVIOURAL RESPONSE TO AMBIENT CURRENTS IN DEMOSPONGES _________ 47 v 3.1 Introduction ____________________________________________________________ 47 3.2 The importance of mesh size and volume flow rates ____________________________ 49 3.3 Methods _______________________________________________________________ 50 3.3.1 Overview __________________________________________________________ 50 3.3.2 Field and lab studies _________________________________________________ 53 3.3.2.1 Measurements of excurrent velocity ________________________________________ 55 3.3.2.2 Measurements of oxygen consumption ______________________________________ 56 3.3.2.3 Test of passive flow _____________________________________________________ 56 3.3.2.4 Statistical analyses ______________________________________________________ 57 3.3.3 Morphometric analysis of sponges _______________________________________ 58 3.3.3.1 Scanning electron microscopy _____________________________________________ 58 3.3.3.2 Histology _____________________________________________________________ 58 3.3.3.3 Measurements of the canal system _________________________________________ 59 3.3.3.4 Estimating resistance through the canal system ________________________________ 60 3.4 Results ________________________________________________________________ 63 3.4.1 Experimental work ___________________________________________________ 63 3.4.1.1 Volume flow rates and oxygen removal _____________________________________ 63 3.4.1.2 Effect of ambient flow on pumping rates _____________________________________ 66 3.4.2 Estimating the cost of filtration _________________________________________ 66 3.5 Discussion _____________________________________________________________ 80 3.5.1 The cost of pumping __________________________________________________ 83 3.5.2 Response to ambient currents __________________________________________ 85 3.5.3 General conclusions __________________________________________________ 86 3.5 References _____________________________________________________________ 87 Chapter Four A GENERAL DISCUSSION ON FILTER FEEDING IN SPONGES
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