University of Plymouth PEARL https://pearl.plymouth.ac.uk 04 University of Plymouth Research Theses 01 Research Theses Main Collection 2016 COMBINED EFFECTS OF OCEAN ACIDIFICATION, OCEAN WARMING AND OIL SPILL ON ASPECTS OF DEVELOPMENT OF MARINE INVERTEBRATES Arnberg, maj http://hdl.handle.net/10026.1/5287 Plymouth University All content in PEARL is protected by copyright law. Author manuscripts are made available in accordance with publisher policies. Please cite only the published version using the details provided on the item record or document. In the absence of an open licence (e.g. Creative Commons), permissions for further reuse of content should be sought from the publisher or author. COMBINED EFFECTS OF OCEAN ACIDIFICATION, OCEAN WARMING AND OIL SPILL ON ASPECTS OF DEVELOPMENT OF MARINE INVERTEBRATES by MAJ ARNBERG A thesis submitted to Plymouth University in partial fulfilment for the degree of DOCTOR OF PHILOSOPHY School of Marine Science and Engineering Faculty of Science and Technology In collaboration with; International Research Institute of Stavanger (IRIS) Stavanger, Norway. University of Gothenburg, Sweden. JANUARY 2016 1 COMBINED EFFECTS OF OCEAN ACIDIFICATION, OCEAN WARMING AND OIL SPILL ON ASPECTS OF DEVELOPMENT OF MARINE INVERTEBRATES By Maj Arnberg i. Abstract For decades, humans have impacted marine ecosystems in a variety of ways including contamination by pollution, fishing, and physical destruction of habitats. Global change has, and will, lead to alterations in in a number of abiotic factors of our ocean in particular reduced oxygen saturation, salinity changes, elevated temperature (ocean warming or OW) and elevated carbon dioxide (ocean acidification or OA). Now and in the future, OA and OW will operate together with local anthropogenic drivers such as oil pollution. And yet, at present, very little is known about their potential combined interactive effects on physiological performance and tolerance of marine organisms. Therefore, multiple driver experiments are required if we are to understand and predict future vulnerability of species, populations and ecosystems. Early life stages of invertebrates are generally considered most vulnerable to environmental stress. However, few studies consider the combined effects OA and OW on survival and growth during early development of marine invertebrates, and to our knowledge, there is no information on the additional effects of oil pollution. Therefore, the aim of this thesis was to investigate the effects of combined exposure to OA, OW, and incorporating local drivers such as oil pollution on the development, morphology and physiology of three economically and ecologically important marine invertebrates. These are Northern shrimp Pandalus borealis, Northern krill Meganyctiphanes norvegica, and the green sea urchin Strongylocentrotus droebachiensis. All are cold-water species, assumed to have a narrower tolerance than more temperate species, and so could be particular sensitive to combined stressor affects. 2 Both Northern krill and to a lesser extent Northern shrimp larvae survived experimental conditions, mirroring those predicted under a future global change scenario (combined OA and OW exposure). Neither was hatching success affected. Both shrimp and krill larvae exhibited accelerated developmental rates and incurred greater maintenance costs as a result of exposure to these stressors. Shrimp larvae showed accelerated developmental rates (-9 days), increased metabolic rates (+20 %), and increased feeding rates (+20 %), but reduced growth (- 9 %) when exposed to OW compared with the control. OA increased development rate but only at the control temperature. Although juvenile mortality of krill was not affected by predicted OA/OW conditions, metabolic rate increased significantly (+ 36 %), as did larval developmental rate, while number of moults, feeding rate and growth (- 67 %) decreased significantly (- 67 %, - 60 % and -8 % respectively). Accelerated development was accompanied by greater maintenance costs possibly due to experience a mismatch between energy supply and demand. Both species had an excess of food, and so growth reduction was more likely to be associated with higher metabolic demands in the future global change treatments. Food shortage in situ, due to variable food availability in the sea and/or mismatch with key prey species (algae and zooplankton) could result in more negative effects on growth and ultimately survival. Green sea urchins were also able to survive OA exposure, without detectable effects on hatching success. However, at day 44 post-fertilization, larval body length in the OA treatment was 9 % lower compared to the control. Furthermore, there was a significant tendency of urchin larvae to increase swimming activity in the OA conditions that might indicate compensatory feeding. Elevated maintenance and repair costs as a result of exposure to multi-stressors affected the energy budget of all the three species studied here resulting in reduced growth. Global drivers (OA and OW) resulted in trade-offs with more energy reallocated to swimming activity and metabolism, rather than growth. Exposure to oil reduced the acquisition of energy by reduced feeding which in turn resulted in less energy being available for growth. Both shrimp and sea 3 urchin larvae showed reduced activity and feeding when exposed to oil. It is possible that the reduced swimming activity observed may be due to a narcotic effect of the oil. Furthermore, early stage sea urchin larvae showed increased mortality when exposed to oil while the older larvae did not, indicating a stage specific toxicity to oil for sea urchin larvae. The combination of global drivers and oil pollution acted additively on growth for both sea urchin and shrimp larvae. The impact of combined drivers on the size of shrimp larvae was equal the sum of the negative impacts observed for each driver: a 5 % reduction when exposed to OA and OW, a 9 % reduction when exposed to oil, and a cumulative 15 % reduction when exposed to all stressors. Similarly, the impact of combined drivers on the size of sea urchin larvae was equal to the sum of the negative impacts observed for each driver: a 14 % reduction when exposed to OA, a 9 % reduction when exposed to oil, and a 21 % reduction when exposed to all drivers. Therefore, the study demonstrated the additive physiological effects of OA, OW and a contaminant, and indicated that larval (sea urchin and shrimp) resilience to future changes (i.e. pollution) could be greatly reduced if larvae were already energy limited and severely stressed (reduced development) as a result of exposure to the global drivers. This study therefore shows the importance that the effective management of local drivers such as oil pollution could have against the backdrop of OA and OW, and emphasises that it is important to study impacts of toxicants, such as an oil pollution, in the context of predicted changes in the environment, as OW and OA are becoming major concerns. Finally, the fact that some local and global drivers seem to act additively should encourage local managers to act on local driver regulations, to obtain positive effects on local populations and environment and thereby rendering them more resilient to the negative impacts of future global drivers. 4 ii. Contents i. Abstract………………………………………………………………………….....2 ii. Contents………………………………………………………………………........5 iii. Abbreviations……………………………………………………………………..10 iv. Figure legends…………………………………………………………………….11 v. Table legends……………………………………………………………………..18 vi. Appendix legends………………………………………………………………....19 vii. Acknowledgements……………………………………………………………….24 viii. Author’s declaration………………………………………………………………26 1. Chapter 1 – General introduction………………………………………………….28 1.1 BACKGROUND…………………………………………………………………28 1.1.1 Ocean acidification, ocean warming and oil pollution – future………….28 oceans will suffer from environmental pressures from several anthropogenic drivers 1.1.2 Development of invertebrate larvae, stress, homeostasis and……………32 energy budget 1.1.3 Impact of OA and OW on marine invertebrate development……………..37 1.1.4 Impact of oil pollution on marine invertebrate development…………………................................................................................41 1.1.5 Impact of multiple drivers on marine invertebrate development…………...44 1.2 THESIS AIMS AND OBJECTIVES……………………………………………..46 1.2.1 Background……………………………………………………………….46 1.2.2 Overall aim………………………………………………………………..47 1.2.3 Aims and objectives of individual chapters………………………………49 1.3 TEST CONDITIONS/RESEARCH FACILITIES……………………………….52 1.4 STUDY SPECIES………………………………………………………………...53 1.4.1 Northern shrimp (Pandalus borealis)…………………………………….53 1.4.2 Northern krill (Meganyctiphanes norvegica)……………………………..56 1.4.3 Green sea urchin (Strongylocentrotus droebachiensis)…………………..58 1.5 COLLECTION SITES……..……………………………………………………..60 5 2. Chapter 2 – Combined effects of decresed pH and ocean warming on …………61 development feeding and metabolism of Northern shrimp (Pandalus borealis) larvae 2.1 SUMMARY………………………………………………………………………61 2.2 INTRODUCTION………………………………………………………………..62 2.3 MATERIALS AND METHODS…………………………………………………64 2.3.1 Adult animal collection and maintenance………………………………...64 2.3.2 Experimental design and set-up…………………………………………..65 2.3.3 Larval collection and maintenance………………………………………..66 2.3.4 Development of shrimp larvae……………………………………………67 2.3.5 Feeding experiment……………………………………………………….68 2.3.6 Determination of metabolic rates…………………………………………69 2.3.7 Statistical