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Ecological Drivers of Jellyfish Blooms – the Complex Life History

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Ecological Drivers of Jellyfish Blooms – the Complex Life History bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 file: Manuscript.docx 22 Feb 2019 2 3 Ecological drivers of jellyfish blooms – the complex life history 4 of a cosmopolitan medusa (Aurelia aurita) 5 6 7 8 J. Goldstein* a, c, U.K. Steiner b, c 9 10 aMarine Biological Research Centre, Department of Biology, University of Southern Denmark, 11 Hindsholmvej 11, 5300 Kerteminde, Denmark 12 bCenter on Population Dynamics, Department of Biology, University of Southern Denmark, 13 Campusvej 55, 5230 Odense, Denmark 14 cMax-Planck Odense Center on the Biodemography of Aging, Department of Biology, University 15 of Southern Denmark, Campusvej 55, 5230 Odense, Denmark 16 17 *Corresponding author: [email protected] 18 19 20 21 Running head Drivers of jellyfish blooms 22 23 1 bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 Summary 25 1. Jellyfish blooms are conspicuous demographic events with significant ecological 26 and socio-economic impact. Despite worldwide concern about an increased 27 frequency and intensity of jellyfish mass occurrences, predicting their booms and 28 busts remains challenging. 29 30 2. Forecasting how jellyfish populations may respond to environmental change 31 requires taking into account their complex life histories. Metagenic life cycles, 32 which include a benthic polyp stage, can boost jellyfish outbreaks via asexual 33 recruitment of pelagic medusae. 34 35 3. Here we present stage-structured matrix population models with demographic 36 rates of all life stages of the cosmopolitan jellyfish Aurelia aurita s. l. for different 37 environments. We investigate the life stage-dynamics of such complex 38 populations to illustrate how changes in medusa density depend on non-medusa 39 stage dynamics. 40 41 4. We show that increased food availability is an important ecological driver of 42 jellyfish mass occurrence, as it can shift the population structure from polyp- to 43 medusa-dominated. Projecting populations for a winter warming scenario 44 additionally enhanced the booms and busts of jellyfish blooms. 45 2 bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 46 5. We identify demographic key variables that control the intensity and frequency of 47 jellyfish blooms in response to anthropogenic drivers such as habitat 48 eutrophication and climate change. By contributing to an improved understanding 49 of mass occurrence phenomena, our findings provide perspective for future 50 management of ecosystem health. 51 52 53 Key-words biodemography, environmental change, jellyfish blooms, matrix model, 54 population structure 55 56 57 Introduction 58 The diversity, productivity and resilience of marine ecosystems worldwide are threatened 59 by an imbalance in the ecological parameters regulating population outbreaks. Mass 60 occurrences of micro- and macroalgae, cnidarians, ctenophores, gastropods, echinoderms, 61 tunicates and fish appear with increased frequency, intensity and geographical 62 distribution (Breithaupt, 2003; Enevoldsen, 2003; Fabricius, Okaji, & De’Ath, 2010; 63 Haddad Junior, Virga, Bechara, Silveira, & Morandini, 2013; Maji, Bhattacharyya, & Pal, 64 2016; Shiganova et al., 2001; Turner, 1994; Vargas-Ángel, Godwin, Asher, & Brainard, 65 2009). Despite being a widespread phenomenon which may serve as an indicator for 66 marine ecosystem degradation, mass occurrence is poorly understood and challenging to 67 predict (Van Dolah 2000). Jellyfish blooms are a prominent example for outbreaks in 68 which the population density of one life stage, the medusa, shows distinct peaks over 3 bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 69 broad temporal and regional scales (Lucas, Graham, & Widmer, 2012). Jellyfish 70 populations, i.e. aggregations of the medusa stage, have increased in numerous coastal 71 regions around the world over recent decades (Brotz, Cheung, Kleisner, Pakhomov, & 72 Pauly, 2012). Such increase has lasting ecological, economic and social implications. 73 Jellyfish blooms can trigger trophic cascades in pelagic food webs due to their severe 74 predatory impact on a broad spectrum of zooplankton species and fish larvae 75 (Richardson, Bakun, Hays, & Gibbons, 2009; Riisgård, Andersen, & Hoffmann, 2012; 76 Schneider & Behrends 1994, 1998). Further, jellyfish mass occurrences can interfere with 77 human activities such as tourism, fisheries, aquaculture and power production (Purcell, 78 2012; Purcell, Uye, & Lo, 2007). Concern about a global rise in jellyfish populations is 79 widespread (Sanz-Martín, Pitt, Condon, Lucas, Novaes de Santana, & Duarte, 2016), as 80 jellyfish outbreaks are thought to be favored by anthropogenic influences; in particular 81 overfishing, eutrophication, habitat modification, species translocation and climate 82 change (Purcell, 2012; Richardson, Bakun, Hays, & Gibbons, 2009). 83 Species that form jellyfish blooms are primarily found within the cnidarian taxon 84 Scyphozoa and feature complex life histories (Hamner & Dawson, 2009). Their 85 metagenic life cycles typically include a pelagic, sexually reproducing medusa and a 86 benthic, asexually reproducing polyp stage (Lucas, Graham, & Widmer, 2012). Such life 87 cycles facilitate mass occurrence and are characterized by high stage-specific plasticity to 88 changing environmental conditions (e.g. Fu, Shibata, Makabe, Ikeda, & Uye, 2014; 89 Gröndahl, 1989; Hamner & Jenssen, 1974; Liu, Lo, Purcell, & Chang, 2009). Although 90 the development of medusa populations is directly linked to survival rates of the planula, 91 polyp and ephyra stage (Lucas, 2001), information on the demographic rates of bloom- 4 bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 92 forming jellyfish has remained scarce (Xie, Fan, Wang, & Chen, 2015). Quantifying 93 demographic rates of all stages in the life cycle of species showing mass occurrence is 94 thus fundamental to identify the environmental variables causing changes in population 95 dynamics and structure. 96 Here, we use the common jellyfish Aurelia aurita s. l. (Linnaeus, 1758) to explore the 97 demographic structure and environmental drivers underlying mass occurrence of a 98 cosmopolitan jellyfish species. We quantify demographic rates of all life stages of A. 99 aurita (larvae, polyps, ephyrae and medusae), i.e. survival, stage-transitions and 100 fecundity, based on experimental and field data. Using these demographic rates, we 101 parameterize stage-structured population models to project the life cycle of jellyfish 102 populations for low and high food levels relating to prey availability in two contrasting 103 temperate water systems. We further predict the impact of a winter warming scenario on 104 the demographic dynamics of A. aurita. Our results provide novel insights into the 105 development of metagenic jellyfish populations under increased food levels and increased 106 winter temperatures. Such information is essential to assess the boosting potential of 107 environmental drivers on species showing mass occurrence and provides a milestone for 108 identifying and managing demographic irregularities in marine ecosystems. 109 110 Materials and Methods 111 Study organism 112 The common jellyfish A. aurita s.l. (Scyphozoa, Cnidaria) belongs to an ubiquitous, 113 cosmopolitan genus with several species and subspecies (Dawson, 2003). Aurelia aurita 114 is well-studied and occurs in a variety of coastal and shelf sea environments, particularly 5 bioRxiv preprint doi: https://doi.org/10.1101/102814; this version posted February 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 115 in northwestern Europe, the Black Sea, Japan and parts of North America (Lucas, 2001). 116 Its life history, i.e. individual stage-trajectory, is subject to a complex life cycle (Fig. 1a) 117 which involves pelagic medusae that reproduce sexually and benthic polyps that 118 reproduce asexually. After sexual maturation, medusae produce large numbers of planula 119 larvae (Ishii & Takagi, 2003), which spend 12 h to 1 week in the water column (Lucas, 120 2001) before they settle and metamorphose into polyps on suitable hard substrate (Holst 121 & Jarms, 2007; Keen, 1987). Polyps reproduce asexually by several modes, including i) 122 the production of well protected chitin-covered resting stages called podocysts (Arai, 123 2009), ii) budding of new polyps (Ishii & Watanabe, 2003), and iii) the release of ephyrae 124 through polydisc strobilation. After asexual propagation,
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