Complete Thesis

University of Groningen Flexible filter feeders van Walraven, Lodewijk IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2016 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): van Walraven, L. (2016). Flexible filter feeders: The gelatinous zooplankton community in the Netherlands after the invasion of the ctenophore Mnemiopsis leidyi. Rijksuniversiteit Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). 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Download date: 09-10-2021 Flexible filter feeders The gelatinous zooplankton community in the Netherlands after the invasion of the ctenophore Mnemiopsis leidyi Lodewijk van Walraven This research was carried out at the Marine Ecology/Coastal Systems department of the Royal Netherlands Institute for Sea Research (NIOZ) in collaboration with Deltares. The study was funded by Stichting Deltares and Royal NIOZ (GELMESOZOO- PLANKTON project) and the EU Interreg IVa 2seas project “MEMO: Mnemiopsis Ecology and Modeling: Observation of an invasive comb jelly in the North Sea” This thesis should be cited as: Van Walraven, L. (2016) Flexible filter feeders: the gelatinous zooplankton community in the Netherlands after the invasion of the ctenophore Mnemiopsis leidyi. PhD Thesis, University of Groningen, Groningen, Printed by GVO Drukkers & Vormgevers, Ede. ISBN: 978-90-367-9294-3 Design, figures and photos by Lodewijk van Walraven unless specified otherwise. Flexible filter feeders The gelatinous zooplankton community in the Netherlands after the invasion of the ctenophore Mnemiopsis leidyi Proefschrift ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen op gezag van de rector magnificus prof. dr. E. Sterken en volgens besluit van het College voor Promoties. De openbare verdediging zal plaatsvinden op vrijdag 18 november 2016 om 14.30 uur door Lodewijk van Walraven geboren op 25 maart 1986 te Warnsveld Promotor Prof. dr. T. Piersma Copromotores Dr. ir. H.W. van der Veer Dr. V. Langenberg Beoordelingscommissie Prof. dr. K.R. Timmermans Prof. dr. M. Boersma Prof. dr. F. Boero Contents I Gelatinous zooplankton in changing Dutch coastal waters 1 Chapter 1 Introduction 3 Chapter 2 Long-term patterns in 50 years of scyphomedusae catches in the western Dutch Wadden Sea in relation to climate change and eutrophication 23 Chapter 3 Where are the polyps? Molecular identification, distribution and population differentiation of Au- relia aurita jellyfish polyps in the southern North Sea area. 51 Chapter 4 Seasonal occurrence of the invasive ctenophore Mnemiopsis leidyi in the western Dutch Wad- den Sea 75 Chapter 5 Changes in the gelatinous zooplankton community in the Dutch Wadden Sea following the invasion of the ctenophore Mnemiopsis leidyi 93 II Invasion success of Mnemiopsis leidyi investi- gated 119 Chapter 6 Mechanisms behind the metabolic flexibility of an invasive comb jelly 121 Chapter 7 Ctenophores invading Amsterdam: Differential response to different salinity levels in two invasive Mnemiopsis leidyi populations 143 Chapter 8 Trophic overlap of the invasive ctenophore Mne- miopsis leidyi with other zooplanktivores in the western Dutch Wadden Sea 165 v Chapter 9 Synthesis 185 Appendix A The use of trichloroacetic acid fixation and propy- lene phenoxetol conservation in quantitative sam- pling of ctenophores 201 Appendix B Identification key for ctenophora in Dutch coastal waters 209 References 213 Summary 243 Samenvatting 247 About the author 253 Acknowledgements 255 Addresses of co-authors 258 List of publications 263 vi Part I Gelatinous zooplankton in changing Dutch coastal waters 1 Chapter 1 Introduction Lodewijk van Walraven 3 Chapter 1 Jellyfish? When most people think of jellyfish, they probably mean the large, conspicuous Scyphomedusae that sometimes wash up on the beach in massive numbers. These have attracted attention of naturalists for centuries. The occurrence of jellyfish on Dutch shores is already mentioned as early as the 16th century. One of the oldest works on marine life in the Dutch language is the the 16th century “Vis- boek” (Fish-book), written and illustrated by beachcomber and fisherman Adriaen Coenen in 1577−1581 (Egmond, 2005). In his book Coenen includes drawings of several species of jellyfish which he calls “zeenetels”, sea-nettles in Dutch. Coenen mentions jellyfish as being “useless creatures” whose bad-smelling corpses were thrown on the beaches and who clogged up fishermen’s net by sticking to the mesh, numbing the hands of the fishermen that had to remove them. On their origin he remarked “When they die they turn to water again, from which they originated”. Probably the earliest study of the seasonal patterns and abundance of jellyfish along the Dutch coast was by Van Deinse (1924) who counted them during beach visits from 1915–1917. The overall abundance trend of jellyfish (Fig. 1.1) showed highest abundances in June–October. The most abundant species found were Aurelia aurita and Rhizostoma octopus. Also here jellyfish are mentioned as causing problems, as in summer sea baths had to be closed when “enormous amounts of jellyfish occurred”. Figure 1.1: Seasonal abundance of jellyfish on Dutch beaches 1915–1917 with months Jan– Jan on the x-axis. Reproduced from Van Deinse (1924). Nowadays most people still seem to think of jellyfish as nuisance species. World- wide, concerns have been raised that jellyfish and jellyfish-related problems are increasing in response to various human-induced stressors (reviewed below). Are jellyfish abundances really increasing? And what will happen with projected climate change? This thesis aims to enhance our understanding of the role of jellyfish in Dutch coastal waters in general and that of an invasive species, the ctenophore Mnemiopsis leidyi, in particular. In the introduction, a short summary of gelati- 4 Introduction nous zooplankton feeding and life cycles is provided first, as there are major differ- ences between taxa. An overview of the role of jellyfish in ecosystem structure and function is given. Following this, an overview of available knowledge on gelatinous zooplankton in Dutch coastal waters is presented and the outline of the thesis is described. “Gelatinous zooplankton” or “gelata” are terms used to describe animals from many different phyla, such as medusae, ctenophores, molluscs, urochordates (salps) and worms. Gelatinous zooplankton are widespread and species of the different phyla can be found in waters ranging from the tropics to the poles (Had- dock, 2004; Lucas and Dawson, 2014). Aside from having a (semi) transparent, fragile body, these animals differ in many ways from each other, and often have entirely different feeding and reproductive strategies. In this chapter the ecology of the three most abundant gelatinous zooplankton groups in Dutch waters is summarised. Ctenophora Ctenophora are the second oldest known multicellular animals to diverge, after Porifera. The alternative hypothesis that Ctenophora are the oldest known multicellular animals to diverge (Ryan et al., 2013), which would imply several independent gains and losses of key metazoan characteristics, is currently not supported (Pisani et al., 2015). 242 species of ctenophores have been described (Zhang, 2011). Cteno- phores have a bi-radially symmetric body with a mouth on one polar end connected to a pharynx and stomach, and subsequently to the anal pore at the other polar end where the statocyst (sensory organ) is also located. Digested food is distributed through the body by means of eight meridional canals, along which the gonads lie in two bands. Also along the meridional canals lie the comb rows which are short, transverse plates of fused cilia arranged in succession. These comb rows are used for locomotion (Ruppert and Barnes, 1994). Different feeding strategies are used (Costello and Coverdale, 1998). Cydippid ctenophores such as Pleurobrachia pileus are sit-and-wait predators and use long, branched tentacles containing colloblasts, sticky adhesive cells to which the prey adheres. Others such as the lobate ctenophore Mnemiopsis leidyi are filter feeders which use rows of cilia on auricules near the mouth to generate a feeding current which gets passed along surfaces lined with colloblasts. Beroid ctenophores such as Beroe gracilis are actively searching predators of other ctenophores. They either engulf the prey whole, or bite off parts (Fig. 1.2). Ctenophores are simultaneous hermaphrodites, having

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