Antagonistic and Synergistic Effects of Ocean Acidification and Global Warming on Sharks

Jennifer C.A.  Pistevos(1), Ivan Nagelkerken(1), Tullio Rossi(1), Maxime Olmos(2), Sean Connell(1)


1 1Southern Seas Ecology Laboratories, School of Biological Sciences and The Environment Institute, The University of Adelaide, South Australia 5005, Australia

2 ENSAIA, 2 Avenue de la Forêt de Haye TSA 40602 54518 Vandoeuvre-les-Nancy, France


Background: Apex predators typically exert substantial top-down forcing on trophically structured food webs, but there is lack of understanding how this function might be altered due to global change. In particular, the combined effect of elevated temperature on metabolism and of elevated CO₂ on the behaviour of larger predators may not only affect their foraging behaviour, but also the communities in which their prey live.

Methods: We used a factorial design in both long-term laboratory and mesocosm studies to assess how warming and ocean acidification affect development, growth, swimming activity, feeding and hunting behaviour in a mesopredator shark.

Findings: Our results showed that the projected increases in ocean temperature and CO2 are likely to act synergistically on predators by not only increasing energetic demands, but also decreasing metabolic efficiency and reducing food intake. Additionally, although temperature increased motivational drive to locate prey, elevated CO₂ negated olfactory and visual behavioural responses that enable effective hunting. Fundamental to these effects was the negligible effect of CO2 in isolation, but its power to negate the positive effects of temperature when brought in conjunction.

Conclusions: The reduced potential to locate prey due to the interactive effects of ocean acidification and warming, in combination with increases in energetic demand, suggests that energetic trade-offs will be needed for sharks to sustain themselves at an individual and population level in a future ocean. Alteration in growth and feeding of predators has important implications for the health and functioning of ecosystems.

40. The impact of high pCO2, both static and fluctuating, on whole-organism thermal tolerance

Robert P. Ellis (1)*, Mauricio A. Urbina (1,2), Cameron Hird (1), Ceri Lewis (1)

1 Department of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK
2 Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile

Organisms’ thermal tolerance has traditionally been used as a predictor of the effect of climate change on species distributions. However, CO2-driven climate change is occurring alongside a parallel increase in seawater pCO2 which is driving ocean acidification. In many coastal regions these changes in pCO2 are not occurring as stable linear decreases over time, but manifest as highly dynamic, fluctuating conditions over a range of temporal and spatial scales. It is not yet fully understood how increases in pCO2, and hence OA, influence an organisms thermal tolerance, and therefore accurately projecting shifts in species distribution due to climate change remains challenging. Consequently, understanding how any complex fluctuations in pCO2 influence thermal tolerance of marine organisms is key for accurately predicting the impact of climate change on future species distributions.

We exposed the harbour ragworm, Hediste diversicolor, to one of four pCO2 regimes for 14 days prior to monitoring metabolic rate and upper and lower thermal tolerance (CTmax and CTmin). Treatments were chosen to represent ambient (400 µatm static), 2100 RCP 8.5 (950 µatm static) and 2300 A2 (1900 µatm static) emissions scenarios. Furthermore a fluctuating treatment (cycling between 400 µatm and 1900 µatm representing a semidiurnal tidal cycle) was included.

These experiments show that both metabolic rate and organismal thermal tolerance were significantly affected by seawater pCO2, and moreover the pCO2 regime (static or fluctuating) affected the magnitude of worms’ responses to high CO2 perturbations.

Understanding the impact of pCO2 on thermal tolerance is a key component for accurately projecting/modelling shifts in species distribution in a changing ocean. Moreover for an accurate representation of this effect we have shown that incorporating measures of fluctuating pCO2 regimes over different temporal or spatial scales is vital.

14. Studies of Ocean Acidification impacts on Antarctic krill at the Australian Antarctic Division

So Kawatuchi (1,2)*, Rob King (1), Natasha Waller (1), Blair Smith (1), Ashley Cooper (1)

1 Australian Antarctic Division, Kingston, Tasmania, 7050, Australia
2 Antarctic Climate & Ecosystems Cooperative Research Centre, Hobart, Tasmania, 7001, Australia

Antarctic krill (hereafter krill) plays a key role in the Southern Ocean (SO) ecosystem being both the primary prey for most of the Antarctic mega fauna and important grazer of the primary production. How krill population may respond to environmental change including ocean acidification is an important management question for the future SO ecosystem, yet very little is known about the sensitivity of krill to ocean acidification. The Australian Antarctic Division (AAD) operates the only research aquarium where krill have been reared and successfully reproduced in captivity for research purposes. It has been conducting various international collaborative experiments on krill biology, physiology, behaviour, including impacts of ocean acidification on krill life history.

The aquarium system has a capacity to allow a range of experimental treatments, with 6 different levels of pCO2 and 3 levels of temperature, with 3 replicates. Experiments are being undertaken in various tank setups (250mL jars up to 200L tanks depending on the nature of the experiments). Krill at various life stages are being tested for various life history parameters such as hatch rates, development and growth parameters, mortality.

Our results so far collectively suggest that the early life stage (embryo) is the most vulnerable to increasing levels of pCO2, with their successful development showing sharp decline above 1250 atmpCO2, and showing zero hatch rate at 2000 atmpCO2. Results on the combined effects of elevated pCO2 and temperature on embryonic development are also expected to be presented.


The AAD has established a state of the art research aquarium for krill and is the only dedicated laboratory for experimental biology of krill outside the Antarctic continent. Our aim is to provide a comprehensive evaluation of the impacts of ocean acidification and warming on krill life history.

13. Response of the photosynthetic rate of macrophytes to increased CO2 concentrations in a brackish-water ecosystem

Pajusalu Liina*, Martin Georg, Põllumäe Arno, and Paalme Tiina

Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618 Tallinn, Estonia

The future increasing CO2 concentrations together with eutrophication and the predicted warming of seawater will create multiple threats to the coastal ecosystems of the Baltic Sea. Macrophytes are important structural component in the shallow coastal Baltic Sea ecosystems. However, their response to acidification and climate change is not well understood. The aim of the current study was to assess whether partial pressure of carbon dioxide (pCO2) and different environmental factors exerted interactive effects on the photosynthesis of key macrophyte species. The second objective examines the short-term variability of carbonate chemistry in shallow-water macroalgal habitats. The field experiments were conducted in Kõiguste Bay (northern part of Gulf of Riga, the Baltic Sea) during vegetation seasons of 2011-2014. Separate mesocosms were maintained at different pCO2 levels: ~2000, ~1000 and ~200 µatm. We measured the short-term photosynthetic responses of four macroalgal species: Fucus vesiculosus, Furcellaria lumbricalis, Ulva intestinalis, Cladophora glomerata and seagrass: Zostera marina. Our results show that increased CO2 levels may enhance the photosynthetic rate of macrophyte species and suggest that predicted marine acidification of the Baltic Sea could have implications for interspecific competition and structure of benthic communities in a future high CO2 world. Daily pH fluctuations may be larger than 1 unit in a shallow-water macrophyte meadow in summer conditions. These daily pH changes may be of a larger magnitude than the scenario modeling suggests for the surface–water pH decrease in the Baltic Sea by 2100.

12. Living in the boundary layer of kelp blades: refuge from ocean acidification or training for harsh conditions?

Fanny Noisette (1), Catriona Hurd (1)*

1 Institute for Marine and Antarctic Studies, University of Tasmania, 20 Castray Esplanade, Battery Point, 7004 TAS Hobart, Australia

Seaweeds are able to modify the chemical environment at their surface, in a micro-zone called the diffusive boundary layer (DBL) via their metabolic processes controlled by light intensity. Depending the thickness of the DBL, sessile invertebrates such as calcifying bryozoans or tube-forming polychaetes living at the surface of the blades can be affected by the chemical variations occurring in this layer. In the context of ocean acidification, these microhabitats might be considered as a refuge from lower pH during light as photosynthesis temporarily raises the pH to values higher than the mainstream seawater.

The thickness and the characteristics of the DBL were assessed at current day pH 8.1 and that predicted for the end of the century, pH 7.7, and seawater flows (slow: 0.5 and fast: 10 cm s-1) on blades of the kelp Ecklonia radiata. Oxygen and pH profiles from the blade surface to the mainstream seawater were measured with microsensors in both bare blades and blades colonized by the bryozoan Membranipora membranacea.

As predicted, the DBL was thicker in slow than in fast flow. We also assumed that the DBL would thinner on blades colonized by bryozoans whereas actually, their presence increased the DBL by creating their own one in addition to the kelp one. The oxygen concentrations and pH levels in the DBL were affected by the presence of bryozoans and the mainstream pH in different ways depending the flow.

These results show that living in the DBL of the kelps can constitute a refuge from ocean acidification or a training for harsh conditions for calcifying organisms living there, particularly in slow flow conditions.

11. Krill (Euphausia pacifica) Development in the Laboratory is Impaired at Currently Observed pCO2 Levels

Anna K. McLaskey (1)*, Julie E. Keister (1), Paul McElhany (2), M. Brady Olson (3), D. Shallin Busch (4), Mike Maher (2), Amanda K. Winans (1)

1 University of Washington, School of Oceanography, Seattle, WA, 98105, USA
2 NOAA Northwest Fisheries Science Center, Seattle, WA, 98112, USA
3 Western Washington University, Shannon Point Marine Center, Anacortes, WA, 98221, USA
4 NOAA Northwest Fisheries Science Center and Ocean Acidification Program, Seattle, WA, 98112, USA

Euphausiids are a critically important component of marine ecosystems around the world, but ocean acidification (OA) work on euphausiids is limited. Research to date has shown that hatching of Euphausia superba eggs and survival of Nyctiphanes couchii sub-adults are reduced at elevated pCO2 levels. Euphausia pacifica is a dominant and trophically important zooplankton species throughout the North Pacific and the California Current Ecosystem, where naturally low pH conditions occur. The areal and temporal extents of these low pH conditions are expected to increase under OA.

We sampled the vertical distribution of E. pacifica eggs and larvae with simultaneous carbonate chemistry measurements to characterize their exposure in Puget Sound, WA, a large estuary connected to the California Current. We also collected adult females and spawned them under a wide range of pCO2 conditions in the laboratory, tracking hatching success, larval development and survival. Our laboratory experiments were designed to cover the broad range of pH conditions that E. pacifica currently experiences in Puget Sound (pH 8.0, 7.7, 7.4) and may experience in the future (pH 7.3, 7.2).

In Puget Sound, WA, E. pacifica larval stages, particularly the nauplius 2 and metanauplius stages, are found throughout the water column (20-180m), where they are exposed to pH 7.8-7.5. In the laboratory, E. pacifica hatching is robust to a range of pH levels, but larval development and survival are reduced at lower pH; survival from three days post hatch to the calyptopis 2 stage was reduced by an average of 20% at pH 7.69 compared to pH 7.96.

This study indicates that E. pacifica may be living near the limits of its pH tolerance and continued OA could push these organisms past their threshold, with negative consequences for their populations and higher trophic levels.

10. Investigating the Multiplicative Effects of Climate Change on Southern Ocean Phytoplankton

Sarah M. Andrew (1)*, Michael Ellwood (2), Philip Boyd (3)

1 Australian National University, Canberra, ACT, 2602, Australia
2 Australian National University, Canberra, ACT, 2602, Australia
3 University of Tasmania, Hobart, TAS, 7005, Australia

Model projections indicate that light, temperature, iron and pH/CO2 in the Southern Ocean are likely to change simultaneously in the future due to changing climate. The individual effects of these variables on phytoplankton productivity have been extensively researched, however the combined effect on Southern Ocean phytoplankton is uncertain. The physiological response of phytoplankton to individual variables may not predict the combined effect of climate change to their fitness, so this project utilized a multiplicative approach to explore metabolic responses and adaptation strategies of Southern Ocean phytoplankton (diatoms and the haptophyte P. antarctica) to climate change. Fe and light interactions were initially explored in P. antarctica and the two diatom species, Proboscia inermis and Eucampia antarctica and photophysiological measurements revealed key differences between these two taxonomic groups. This study is the first to identify a key process that allows diatoms to photosynthesise at a comparable rate to P. antarctica in spite of their physiological limitations. This project also focussed on increasing CO2 and temperature in addition to the Fe and light experimental incubations using P. antarctica. Addition of Fe in experimental cultures with increased CO2, temperature and light resulted in increased growth rates and colony abundance plus changes in a number of photophysiological characteristics. In contrast, it was found that Fe limitation caused a significant decline in growth and photosynthetic efficiency when combined with increased CO2, temperature and light. The investigation into the antagonistic and synergistic relationships that influence phytoplankton productivity concluded that unknown changes in Fe supply will be the main control on future productivity.

8. Elevated CO2 demonstrates insignificant impacts on bacterial community structure in a subtropical coastal mesocosm experiment

Xin Lin (1)*, Ruiping Huang (1), Yibin Huang (1), Kunshan Gao (1)

1 State Key Laboratory of Marine Environmental Science, Xiamen university, Xiamen, Fujian province, 361100, China
*Corresponding author:

Set within an ecological framework, we investigated the effects of elevated CO2, contrasted with ambient CO2, on dynamics changes of bacterial communities during diatom bloom in a replicated subtropical seawater mesocosm experiment. The mesocosm experiment was conducted in FOANIC-XMU mesocosm platform located in the seawater of Wuyuan Bay, Xiamen, Fujian province, East China Sea (N24°31′48″, E118°10′47″) during the months of December 2014 and January 2015.

The pCO2 in the mesocosms was controlled by bubbling with air of high (HC, 1000 μatm) or low (LC, 395 μatm) pCO2. 16S rRNA V3-V4 region Illumina MiSeq sequencing was used to characterize bacterial(cell diameter is less than 0.2um) community structure dynamics with high taxonomic resolution in this study.

This high-throughput sequencing analysis produced 2365844 clean reads, which comprised 6334 OTUs. The mesocosm bloom significantly changed the bacterial community structure. Initially, all mesocosms were dominated by proteobacteria. Bacteriodete is stimulated by mesocosm bloom later on. Finally, cyanobacteria was the predominant class in the all mesocosms. However, no significant differences between high CO2 treatment and low CO2 treatment were observed in bacterial abundance, community assemblage and composition.

The results demonstrate that marine bacterial community are highly resistant to elevated CO2 and lower pH conditions in subtropical coastal seawater. It is tempting to conclude that there are no direct effects on marine bacterial communities imposed by ocean acidification because marine bacteria in subtropical coastal region hold enough flexibility and capacity to deal with future carbonate system changes caused by elevated CO2 and subsequent ocean acidification.

7. Effect of lower pH on settlement and development of coral, Pocillopora damicornis (Linnaeus, 1758)

Voranop Viyakarn (1), Wipada Lalitpattarakit (1), Narainrit Chinfak (1), Suppakarn Jandang (1), Pataporn Kuanui (1), Somkiat Khokiattiwong (2), Suchana Chavanich (1)*

1 Reef Biology Research Group, Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand
2 Phuket Marine Biological Center, Department of Marine and Coastal Resources, Phuket 83000, Thailand

The effects of pH reduction on the settlement and development of the coral Pocillopora damicornis were investigated. Three different pH treatments (pH = 7.6, 7.9, and 8.1) were used. In addition, water quality (temperature, salinity, total alkalinity) around the study site was monitored. The results showed significant differences in the settlement rates of Pocillopora damicornis larvae between pH treatments (p < 0.05). A decrease in pH levels caused a strong decline in larval settlement rate. In addition, at pH 7.6 and 7.9, all larvae were unable to complete metamorphosis, and metamorphosis delay was observed. Field monitoring showed low fluctuation of all seawater parameters within 24 hours, and there was no difference between seasons. From this study, a strong negative effect of pH reduction on P. damicornis larvae was observed. Although the function of physiology is still not clearly understood, correlations are likely to exist.

6. Will ocean acidification alter thermal windows of echinoderm fertilisation and early development?

Sam Karelitz (1), Sven Uthicke (2), Miles Lamare (1)*

1 University of Otago, Dunedin, Otago, 9016, New Zealand
2 Australian Institute of Marine Science, Townsville MC, PMB No 3, Queensland 4810, Australia

The thermal windows of developmental stages are key drivers of the geographical distribution and abundance of marine invertebrates. If changes in sea temperature and pH interact to affect species in the future, then ocean acidification may influence developmental thermal windows, and may be important considerations under realistic climate change scenarios.

We examined the effects of reduced seawater pH/increased pCO2 on the thermal windows of fertilisation and embryology of three echinoid species; one tropical (Arachnoides placenta), one temperate (Fellaster zelandiae), and one polar (Sterechinus neumayeri). Using a thermal block heated and cooled at each end to create a temperature gradient, developmental responses were examined across 12 temperatures (centered around current ambient temperatures during spawning seasons) ranging from -1.1 to 5.7 C (S. neumayeri), 5.8 to 27 C (F. zelandiae), and 14.1 to 35.3 C (A. placenta) under present (≈450 ppm pCO2) and near future (year 2100) ocean pH/pCO2 (≈900 ppm pCO2) conditions.

The tropical A. placenta had a broader optimum thermal range for successful fertilisation (19 to 32 C) than F. zelandiae (15.8 to 23.4 C) and S. neumayeri (-1.1 to 4.3 C). Neither fertilisation nor the fertilisation window was affected by pH in any of the species. A. placenta and F. zelandiae had broad thermal windows for embryological development (21 to 31C and 10 to 21.4C respectively) compared to S. neumayeri (-1.1 to 1.35C). While pH did slightly reduce normal development of A. placenta, no significant interaction between pH and temperature on embryological development was detected across the thermal window for any of the three species.

The results of this study suggest that in terms of fertilisation and early development, while temperature is an important factor influencing species distribution in future ocean conditions, there was little evidence of an interactive effect of ocean acidification on their specific thermal windows.