Herbivory, phenotypic variation, and reproductive barriers in fucoids Helena Forslund ©Helena Forslund, Stockholm University 2012 Cover illustration: Helena Forslund ISBN 978-91-7447-538-8 Printed in Sweden by US-AB, Stockholm 2012 Distributor: Department of Botany, Stockholm University Live your life filled with joy and wonder Live your life filled with joy and thunder - R.E.M. Doctoral dissertation Helena Forslund Department of Botany Stockholm University SE-106 91 Stockholm Sweden Herbivory, phenotypic variation, and reproductive barriers in fucoids Abstract. Along the shores of the Northern hemisphere Fucus (Phaeophyceae) species are a prominent presence, providing substrate, shelter, and food for many species. Fucus evanescens, a non-indigenous species (NIS) in Sweden, and F. radicans, a recently described species that so far has only been found inside the species poor Baltic Sea, are the focus of this thesis. Interactions with enemies (e.g. predators, herbivores, parasites) have been shown to play a role in the success of NIS. The low consumption of Fucus evanescens by the generalist gastropod Littorina littorea in Sweden was found to depend on high levels of chemical defense in the introduced population, not the failure of the herbivore to recognize F. evanescens as suitable food. A survey of the relative abundance of F. radicans and F. vesiculosus and the most common associated fauna along the Swedish Bothnian Sea coast showed that F. radicans and F. vesiculosus are equally abundant throughout the range of F. radicans. The most common associated fauna were found to be more abundant on F. radicans compared to F. vesiculosus. In Sweden, where F. radicans had lower levels of defense chemicals than F. vesiculosus, F. radicans was grazed more than F. vesiculosus in bioassays. This could, together with other factors, influence the range of F. radicans. Fucus radicans and F. vesiculosus are closely related, recently separated, and growing sympatrically, therefore, possible reproductive barriers between F. radicans and F. vesiculosus were studied. In Estonia F. radicans and F. vesiculosus reproduces at different times of the year. No such clear reproductive barrier was found between the two species in Sweden where they reproduce at the same time and fertilization success and germling survival were the same for hybrids as for F. vesiculosus. Since the high clonality of F. radicans means that the gentic diversity in F. radicans populations is low I investigated how genetic diversity translates to phenotypic diversity in nine traits. Phlorotannin levels, recovery after desiccation, and recovery after freezing showed inherited variation, while the other six traits showed no variation related to genetic diversity. Phenotypic variation in populations of F. radicans will be higher in populations with higher genetic diversity and this might be beneficial to the community. Keywords – Non-indigenous species; Enemy Release Hypothesis; Asexual reproduction; Phlorotannins; Distribution List of papers This thesis is based on the following papers, which are referred to by their roman numerals in the text: I. Forslund H, Eriksson O, Kautsky L (2012). Grazing and geographic range of the Baltic seaweed Fucus radicans (Phaeophyceae). Marine Biology Research 8:322-330. II. Forslund H, Wikström SA, Pavia H (2010). Higher resistance to herbivory in introduced compared to native populations of a seaweed. Oecologia 164:833-840. III. Forslund H, Kautsky L. Reproduction and reproductive isolation in Fucus radicans (Phaeophyceae). Accepted for publication in Marine Biology Research. IV. Johannesson K, Forslund H, Capetillo NÅ, Kautsky L, Johansson D, Pereyra R, Råberg S (2012). Phenotypic variation in sexually and asexually recruited individuals of the Baltic Sea endemic macroalga Fucus radicans: in the field and after growth in a common-garden. BMC Ecology 12. In paper I I planned and performed the study and experiments as well as wrote the paper and did the statistical analyses. For paper II I planned and performed experiments and studies, wrote most of the paper and did the statistical analyses. For paper III I planned and performed the experiments and studies, wrote the text and performed statistical analyses. For paper IV I planned and performed studies and experiments. Paper I and III is reprinted with permission from Taylor and Francis. Paper II is reprinted with kind permission from Springer Science and Business Media. Paper IV is reprinted with permission from BMC Ecology. Content Foreword ........................................................................................................... 10 Introduction ....................................................................................................... 11 The Fucus species studied ............................................................................. 11 Objectives of the thesis ................................................................................. 13 The associated flora and fauna of seaweed beds ......................................... 13 Herbivory and herbivory defense in fucoid algae ......................................... 14 Non-indigenous species and marine introductions ....................................... 15 Reproduction and reproductive isolation in Fucus species ........................... 17 Effects of genetic diversity on resilience and biodiversity in the Fucus community ..................................................................................................... 18 Study area ...................................................................................................... 19 The herbivores ............................................................................................... 21 Studies ............................................................................................................... 21 Surveys of relative abundance of F. radicans and F. vesiculosus and diversity and abundance of the associated fauna ....................................................... 21 Herbivore defense and phlorotannins .......................................................... 22 Reproductive effort and reproductive isolation of F. radicans and F. vesiculosus ..................................................................................................... 24 Genetic diversity and variation in traits in F. radicans .................................. 24 Results and discussion ....................................................................................... 25 Acknowledgements ........................................................................................... 30 References ......................................................................................................... 31 Svensk sammanfattning .................................................................................... 42 Tack! .................................................................................................................. 47 Appendix 1 ......................................................................................................... 49 Foreword Under the surface of the ocean, where this thesis will take you, an alien world meets us. More people have walked on the surface of the moon than in the deepest trenches in the oceans. I hope and expect that we will be endlessly awed by the mysteries that are uncovered as scientists continue to learn more, but also that we will never learn everything there is to know. My astronomy and astrophysics professor would spend hours explaining a single theory for us, only to end the lecture by saying, “Or at least this is what the scientists are saying right now. If you have a better theory I’m willing to listen - what we know might change in a year anyway.” I would step out from the university building into the night and walk home, looking up at the stars and feeling awed by the thought of both everything we do not know and everything we will never understand. Studying biology only increased this sense of wonder but this time the focus was much closer than the stars: my cells, the bacteria on my skin, and the trees outside of my window - each no less amazing or unknown than the cosmos. Over the last decades we have learned that organisms in the ocean that seem to be among the simplest forms of life, the algae, have intricate systems that can measure the moon’s phases, sense light, send warning messages and sense how much the water is moving. We have found that a single genetic individual can be spread over a large area – it is as though thousands of copies of you were living in an area so wide that it would take more than a week to bike through. This thesis focuses on a genus of seaweeds – the Fucus – that are present along temperate shores on the northern hemisphere. Living under water, they exist in an environment that is so foreign to us that it is hard to imagine. They are so different from us that intuition and common sense do not apply to them. They synthesize energy from the sun, they cannot move, and while they might seem like a simple slimy presence along the shores they have intricate systems to sense and react to their environment. 10 Introduction The Fucus species studied Seaweeds of the genus Fucus (Phaeophyceae) are a group of large, perennial brown seaweeds. They are found in temperate and arctic waters on the northern hemisphere. On intertidal rocky shores they usually form a belt with different fucoid species dominating at different shore levels. Pelvetia canaliculata (L.)