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By School of Biological Sciences March 2005 SUNBURNT SEA SNAILS: THE ROLE OF ULTRAVIOLET RADIATION IN THE DEVELOPMENT OF ENCAPSULATED EMBRYOS FROM TEMPERATE ROCKY SHORES * A thesis submitted in fulfilment of the requirements for the award of the degree DOCTOR OF PHILOSOPHY from UNIVERSITY OF WOLLONGONG by RACHEL PRZESLAWSKI, B.A. School of Biological Sciences March 2005 iii THESIS CERTIFICATION CERTIFICATION I, Rachel Przeslawski, declare that this thesis, submitted in fulfilment of the requirements for the award of Doctor of Philosophy, in the School of Biological Sciences, University of Wollongong, is wholly my own work unless otherwise references or acknowledged. The document has not been submitted for qualifications at any other academic institution. Rachel Przeslawski 29 March 2005 iv This thesis is dedicated to Mary Bissonnette without whom I never would have accomplished what I have today. I’m only just starting to realise how much hard work and sacrifice you made over the years, and I’m truly grateful… thanks heaps Mom! v ACKNOWLEDGEMENTS I’m extremely grateful to my supervisors Kirsten Benkendorff & Andy Davis. Kirsten gave me endless encouragement, advice, and great suggestions even from afar. She’s been a wonderful role model, and her enthusiasm for her research is infectious… I’m proud to be her first PhD student! Andy gave me the idea for the initial topic and always had a great knack for stepping back from the little details to see the bigger picture, something that no doubt helped some of these manuscripts get published. He’s also been a great source of information about experimental design, statistics, general marine ecology, and bad puns. Thank you both! I’m also thankful for all the support from my family over the years. Mom, Dad, Mark and Mike all helped instil the knowledge, natural curiosity, and persistence (stubbornness) that drive everything I do today. I’m particularly grateful to Patrick Falvey who supported me financially and emotionally during my research; without his help, this never would have been completed. I can’t think of anyone else who would have run out on a roof in torrential rain with me to ‘rescue’ tiny snotty egg mass pieces in outdoor aquaria! Pat also used his bloody engineering skills for good by helping to construct many of the aquaria and tanks that were used in some of these studies. Walt Dunlap graciously provided his time and expertise to help me create MAA standards for this research. Ken Russell provided his statistical expertise for some of the more complex experimental designs. Peter Middlefart, Todd Minchinton, Jan Pechenik, Winston Ponder, Sharon Robinson, Jeff Wright, Richard Strathmann and several anonymous reviewers all made valuable comments on earlier drafts of the manuscripts and thesis that greatly improved the final products. Bill Rudman, Peter Middelfart, and others in the malacology and fish departments at the Australian Museum helped identify some of the species used here. James Wraith and Amanda Watson helped out with some of my field collecting and experimental set-up. Sharon Robinson helped me with HPLC equipment, and Ross Lilley did the same with spectrophotometry. I’m also grateful to many other staff in the School of Biological Sciences for providing great support and advice during my time there! I’d also like to thank my fellow postgrads, particularly our lab group, for providing advice and commiseration over the years! This work was supported in part through student grants from the Institute of Conservation Biology (U of W), the Malacological Society of Australasia (Chapter 2), the Malacological Society of London (Chapter 3.3), and the Conchologists of America (Chapter 4.2). vii ABSTRACT Ultraviolet radiation (UVR) is an important abiotic stressor for both aquatic and terrestrial organisms. The recent anthropogenic depletion of stratospheric ozone has resulted in elevated levels of potentially damaging UV-B to which organisms are exposed, and global climate change may also herald changes in environmental conditions, particularly temperature, precipitation, and sea level. Thus, organisms may be simultaneously exposed to variable environmental stressors. In the marine environment, embryos and larvae are likely the most vulnerable to the negative effects of these stresses. Moreover, intertidal organisms are particularly vulnerable to UVR because they occur in habitats where little or no UVR is absorbed by the water column, and the effects of UVR are coupled with other potential negative stresses associated with low tides. Surprisingly, little is known about the effects of potential interactions between environmental stressors on marine larvae, particularly involving UVR. This study aims to investigate the role of UVR in the development of encapsulated intertidal embryos through a series of six independent experiments that screen a large number of taxa. In the first four experiments, I explored the direct effects of UVR in isolation and with other stressors (UVR/temperature/salinity and UVR/desiccation), as well as the indirect effects of UVR and fouling. Isolated effects of UVR were investigated on egg masses from 23 marine gastropod species collected from three intertidal habitats (full sun, partial shade, full shade) and exposed to four spectral treatments (full spectrum, no UV- B, no UVR, dark). Embryos from full shade habitats were significantly vulnerable to UVR while those from full sun habitats showed no significant mortality differences between spectral treatments. Multifactorial experiments were then conducted in which encapsulated embryos of three common rocky shore gastropods were exposed to simultaneous combinations of (i) UVR, temperature, and salinity and (ii) UVR and desiccation. Siphonaria denticulata and Bembicium nanum embryos were expected to be tolerant to these negative interactions of stressors as they are routinely deposited on rock platforms exposed to solar radiation. In contrast, Dolabrifera brazieri embryos were predicted to be vulnerable to these stressors as they are deposited in shaded, submerged habitats. I viii detected species-specific synergistic effects of these stressors, and increases in mortality and retardation of development were generally associated with the most physiologically stressful conditions. Based on laboratory results, embryos of D. brazieri were the most sensitive to all the stressors. In contrast, S. denticulata and B. nanum were vulnerable to negative effects associated with synchronous spectral, thermal, and salinity stress; but they were relatively tolerant to UVR and desiccation. Nevertheless, field results indicate that embryos of these species within desiccated habitats have a significantly higher mortality than those within submerged habitats, suggesting that development on rock platform surfaces may not be optimal for these embryos. The indirect effects of UVR and fouling on encapsulated larval development were investigated on egg masses from 18 species cultured under three spectral treatments (full spectrum, no UV, dark). Algal fouling levels, protist colonisation, embryonic mortality, and encapsulation period were recorded, and I found that UVR inhibited algal growth and protist colonisation on egg mass surfaces. Although algal fouling was not directly related to embryonic mortality in most species, egg masses colonised by protists had a higher level of algal fouling; and overall, these egg masses had a significantly higher incidence of embryonic mortality. In the last two experiments, I examined potential behavioural and biochemical protection afforded to encapsulated intertidal embryos against UV-induced damage. I conducted surveys of intertidal egg masses in south-eastern Australia over two years to determine if spatial and temporal variation in parental site selection could reduce potential environmental stress to encapsulated embryos. I predicted that egg masses would be predominantly deposited in shaded habitats not prone to environmental extremes. Furthermore, I anticipated that egg masses deposited on rock platform surfaces would be smaller and occur less frequently in these habitats during seasons of high environmental stress. As predicted, most species spawned under boulders, thereby minimising exposure to environmental stress. Analyses confirmed that summer had the highest UVR index, water temperature, and air temperature, as well as the lowest tides; but assemblages and abundances of egg masses on exposed rock platforms were highest during summer with no change in egg mass sizes. Thus, species spawning on rock platform surfaces do not seem to confer protection to their encapsulated offspring by avoidance of physiologically stressful times or conditions. Alternatively, one or more of ix these potential stressors are beneficial to embryonic development, and these benefits outweigh negative effects. For example, high temperatures associated with direct sunlight may increase developmental rate and counteract any negative effects associated with UVR. Potential biochemical protection against UV-induced damage was examined by quantifying potential chemical suncreens, mycosporine-like amino acids (MAAs), in intertidal egg masses from 46 mollusc species, two polychaete species, and one fish species from southeastern Australia. Analyses revealed that egg mass maturity and spawning habitat did not significantly affect MAA composition within egg masses. In contrast, adult diet, phylogeny, and viability significantly affected MAA composition. Herbivores had significantly higher levels of certain MAAs than carnivores, and viable egg
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