Role of Behaviour in Marine Organisms: Potential Effects Under Future Ocean Conditions
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Dottorato di Ricerca in Scienze della Terra e del Mare Dipartimento di Scienze della Terra e del Mare (DiSTeM) Settore Scientifico Disciplinare: BIO/07 - Ecologia ROLE OF BEHAVIOUR IN MARINE ORGANISMS: POTENTIAL EFFECTS UNDER FUTURE OCEAN CONDITIONS IL DOTTORE IL COORDINATORE DAVIDE SPATAFORA PROF. MARCO MILAZZO IL TUTOR PROF. MARCO MILAZZO CICLO XXXIII 2021 1 Role of behaviour in marine organisms: potential effects under future ocean conditions Il Dottore Il Coordinatore Davide Spatafora Prof. Marco Milazzo Il Tutor Prof. Marco Milazzo 2 3 Index List of papers ....................................................................................................................................... 5 Summary .............................................................................................................................................. 7 Chapter 1 - General Introduction ...................................................................................................... 12 Effects of Ocean Acidification (OA) on marine organisms ............................................................. 16 Effects of Ocean Acidification (OA) at the ecosystem levels ......................................................... 19 Effects of Ocean Warming on organisms and ecosystems ............................................................ 21 Aims and structure of the thesis .................................................................................................... 24 References...................................................................................................................................... 26 Chapter 2 - Plastic adjustments of biparental care behaviour across embryonic development under elevated temperature in a marine ectotherm ...................................................................... 43 Introduction ................................................................................................................................... 43 Materials and Methods .................................................................................................................. 48 Results ............................................................................................................................................ 55 Discussions ..................................................................................................................................... 59 References...................................................................................................................................... 65 Supporting Information ................................................................................................................. 76 Chapter 3 - Nest guarding behaviour of a temperate wrasse differs between sites off Mediterranean CO2 seeps ................................................................................................................ 84 Introduction ................................................................................................................................... 84 Materials and methods .................................................................................................................. 87 Results ............................................................................................................................................ 93 Discussion ....................................................................................................................................... 97 References.................................................................................................................................... 101 Supplementary material .............................................................................................................. 111 Chapter 4 - Limited behavioural effects of ocean acidification on a Mediterranean goby (Gobius incognitus) chronically exposed to elevated CO2 levels ................................................................ 119 Introduction ................................................................................................................................. 119 Materials and Methods ................................................................................................................ 121 Results .......................................................................................................................................... 126 Discussion ..................................................................................................................................... 132 References.................................................................................................................................... 137 Supplementary material .............................................................................................................. 148 Chapter 5 – Concluding remarks and future directions ................................................................. 154 References.................................................................................................................................... 158 4 List of papers Published papers: • Spatafora, D., Massamba N’Siala, G., Quattrocchi, F., Milazzo, M., Calosi, P. (2020). Plastic adjustments of biparental care behaviour across embryonic development under elevated temperature in a marine ectotherm. Ecology and Evolution. DOI: 10.1002/ece3.7902 Papers under review: • Spatafora, D., Quattrocchi, F., Cattano, C., Badalamenti, F., Milazzo, M. (2021). Nest guarding behaviour of a temperate wrasse differs between sites off Mediterranean CO2 seeps. Science of the Total Environment (Under review) • Spatafora, D., Cattano, C., Aglieri, G., Quattrocchi, F., Turco, G., Quartararo, G., Dudemain J., Milazzo, M. (2021). Ocean acidification and behavioural response to predation risk in the Mediterranean goby (Gobius incognitus) living along a vulcanic CO2 gradient off Vulcano Island. Marine Environmental Research (Under review) 5 6 Summary Over the last 250 years, the intensive burning of fossil fuels along with industrial processes and land uses (e.g. clearing forests and agriculture) has contributed to an increase in atmospheric CO2 from approximately 280 to 410 ppm, with a further increase (from 730 to 1020 ppm) projected by the end of this century. About 30% of the anthropogenic CO2 has been absorbed by the ocean, with a consequent decrease of the ocean’s surface pH causing a phenomenon better known as Ocean Acidification (OA). The average pH of the surface ocean has declined from 8.2 by 0.1 units since pre-industrial times as a result of CO2 emissions and a further reduction of 0.3–0.5 pH units is expected to occur by the 2100. This increased concentration of atmospheric CO2 has driven an increase in atmospheric and oceanic temperatures enhanced at a rate of ~ 0.2˚C per decade in the past 30 years. These rapid changing ocean conditions in pCO2 and temperature are considered two of the major threats to marine biodiversity, leading to changes in the distribution, physiology and behaviour of marine organisms, with potential consequences in community and ecosystem functioning and structure. Despite the increasing interest and amount of literature on this topic, the effects of OA and ocean warming (OW) on marine fauna is difficult to predict, especially because a wide range of impacts have been found across different life stages-and species suggesting that tolerance thresholds to such stressors can vary among life stages experienced by an organism or even between species. In this regard, an increased number of studies has been conducted to better understand the mechanisms by which species can cope with these rapid environmental changes. The first response of animals to a changing environment is predominantly through modification of their behaviour. To date, only a few climate change biology studies have considered behavioural plasticity as a way that animals can adjust their performance under rapid climate change, especially for marine ectotherms. 7 The general objective of this thesis was to evaluate the effects of ocean warming and acidification on different aspects of behaviour in marine ectotherms. To achieve this aim I investigated the behavioural responses of two marine fish and one invertebrate, through field-based and laboratory experiments. In Chapter 2 of this thesis, I assessed the plasticity of parental care investment under elevated temperatures in a gonochoric marine annelid with bi-parental care, Ophryotrocha labronica, and investigated its role in maintaining the reproductive success of this species in a warming ocean. I measured the time individuals spent carrying out parental care activities across three phases of embryonic development, as well as the hatching success of the offspring as a proxy for reproductive success, at control (24°C) and elevated (27°C) temperature conditions. Under elevated temperature we observed: (i) a significant decrease in total parental care activity, underpinned by a decreased in male and simultaneous parental care activity, in the late stage of embryonic development; and ii) a reduction of hatching success, that was however not significantly related to changes in parental-care activity levels. These findings, along with the observed unaltered somatic growth of parents and decreased brood size, suggest that potential cost-benefit trade-offs between offspring survival (i.e. immediate fitness) and parents somatic condition (i.e. longer-term fitness