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.

1. Effects of Ocean Acidification on the Growth of juvenile Mytilus edulis

Mary Margaret Stoll (1,3)*, Robert Holmberg (1), Aaron Honig (1,2), and Dr. Robyn Hannigan (1)*

1 School for the Environment, University of Massachusetts Boston, Boston, MA, 02125, USA
2 Biology Department, University of Massachusetts Boston, Boston, MA, 02125, USA
3 Chemistry and Environmental Studies Departments, Amherst College, Amherst, MA, 01002, USA

Ocean acidification is the process in which surplus atmospheric carbon dioxide (CO2(g)) transfers across the ocean-atmosphere boundary and becomes CO2 (aq). This process changes the carbonate system balance leading towards increased [H+] and decreased [CO32-], ultimately causing increased acidity of the water. Furthermore, this changes the saturation state of carbonate minerals, shifting away from stability towards dissolution. As a result, carbonate biominerals such as those in bivalve shells become thermodynamically less stable and may dissolve or shift towards a more stable form.

We grew the juvenile blue mussel, Mytilus edulis, under different CO2-induced low pH conditions to explore the effect of ocean acidification on growth. We used a pH-stat CO2-dosing system designed for ocean acidification research with four replicates per treatment (n=4, control-outside room: pH=8.1, control: pH=8.1, treatment 3: pH=7.6, treatment 4: pH=7.3). We monitored carbonate chemistry parameters including pH, salinity, temperature, and total alkalinity. Juveniles were fed T-Isochrysis algae. We changed the water in each tank everyday and counted algal cells to estimate algal density.

At the end of the one-week exposure, we measured survivorship, shell length and width. We evaluated shell morphometrics using a Matlab script to determine circularity, area and perimeter. There was no difference in mussel growth between treatments (p>0.1). However, there were differences in the circularity of the mussel shells between treatments (p<0.1). Scanning electron microscopy and associated image analysis of the mussel shells indicated variations in the mineralogy and structure of the shell between treatments.

There was no difference in mussel growth between treatments. However, there were differences in the circularity of the shells between treatments. Analysis of the shell structure and mineralogy showed some impacts as well. Though this is a preliminary study, research is on-going to explore these impacts across life stages.

18. Vulnerability of Pteropod Shell In The Arctic Ocean: A Result of Culture Experiment Under Natural Seawater

Katsunori Kimoto (1)*, Jonaotaro Onodera (1), Naomi Harada (1), Kohei Matsuno (2), Takahito Ikenoue (3), Osamu Sasaki (4)

1 Institute of Arctic Climate and Environment Research (IACE), JAMSTEC, 2-15, Natsushima-cho, Yokosuka, 237-0061, Japan.
2 National Institute of Polar Research (NIPR), 10-3, Midori-cho, Tachikawa-shi, Tokyo 190-8518, Japan.
3 Marine Ecology Research Insitiute, 300 Iwawada, Onjuku-machi, Isumi-gun, Chiba 299-5105 Japan.
4 The Tohoku University Museum, 6-3 Aoba, Aramaki, Aoba-ku, Sendai, 980-8578 Japan.

The pteropods (thecosome), planktic molluscs having aragonite shell is major component of marine zooplankton and it plays important roles for oceanic carbon cycles and marine ecosystems. In particular, the aragonite shell is more soluble in seawater, and could be affected by ocean acidification (OA). In this study, we performed simple culture experiment of pteropod Limacina helicina living in the Arctic Ocean and described shell degradation processes under different water mass in the natural seawater.

Culture experiment had carried out on the R/V Mirai during the Leg MR13-06 Arctic cruise in 2013. In this cruise, we stayed two weeks at fixed station (Sta. 41: 72° 45’N, 168°16’W, water depth: 52 m) from 11 Sep. to 25 Sep., 2013 and collected L. helicina by vertical plankton tow for culture experiments. During observations, we observed drastic changes of carbonate chemistry in the water column within several days. In particular, degrees of aragonite saturation (Ωara) was shown from 0.6 (around seafloor) to 2.1 (surface). We used these natural seawater with different three conditions of Ωara (0.7, 1.4, and 2.1), and cultured L. helicina in nine culture vessels (batches) during two weeks.

The texture of shell surface of L. helicina showed remarkable changes under stereomicroscope within 48 hours from starting experiment: All shells of L. helicina kept hyaline under 2.1 and 1.4 of Ωara conditions. On the other hand, cloudy and whitish (damaged) shells were appeared under 0.7 Ωara condition. Seven days after, shell surface became whitish moderately in 1.4 Ωara conditions. It had never appeared whitish colored shells under 2.1 Ωara condition through the period of culture experiment. Onshore laboratory, all cultured shell density of L. helicina had analyzed to detect aragonite shell density by the Microfocus X-ray CT (MXCT). We will discuss about shell density changes during the culture experiment.

39. Adaptive capacity of the sea urchin Heliocidaris erythrogramma to ocean change: responses from fertilisation to the juvenile

Shawna A. Foo (1), Symon A. Dworjanyn (2), Alistair Poore (3), Januar Harianto (1), Maria Byrne (4)*

1 School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia
2 National Marine Science Centre, Southern Cross University, Coffs Harbour, New South Wales, Australia
3 Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia
4 Schools of Medical and Biological Sciences, The University of Sydney, Sydney, New South Wales, Australia

To accurately predict impacts of ocean acidification and warming on the responses of marine populations, it is important to determine an organism’s capacity for phenotypic plasticity and the potential of species for genetic adaptation.

We determined the effects of near-future acidification and warming across the life cycle of Heliocidaris erythrogramma from fertilisation to metamorphosis in the progeny of 16 sire-dam crosses. Sources of variation in tolerance to warming (+3 °C) and acidification (-0.3-0.5 pH units) were investigated for fertilisation, larval success and juvenile metamorphosis.

Across all life stages, maternal legacy was important, with dam identity significantly interacting with stressors. Across the genotypes tested, fertilisation was negatively affected by increased temperature, but not pH. Larval development was compromised in low pH, but not temperature. By the settled juvenile stage, no impact of warming or acidification was evident and this was likely due to selective mortality of sensitive individuals. Across all environments tested, the juveniles exhibited a similar ability to calcify.

The impact of warming and acidification on development after fertilisation was influenced by parental identity, with the offspring of some dam-sire pairs more sensitive than others. That the progeny of some sire-dam pairs showed high stress tolerance indicates the potential for selection of resistant genotypes and adaptation that could facilitate the persistence of H. erythrogramma populations. Performance of progeny at one stage could not predict the performance later in development and shows the importance of assessing impacts of ocean change across the life cycle of marine invertebrates.

17. Two-current choice flumes for fish chemosensory behaviour – method validation and limited effects of high pCO2

Fredrik Jutfelt (1), Josefin Sundin (2), Graham D Raby (3), Timothy D Clark (4)

1 Norwegian University of Science and Technology, Trondheim, 7491, Norway
2 Uppsala University, Uppsala, 751 24, Sweden
3 Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, N9C1A2, Canada
4 University of Tasmania and CSIRO Agriculture Flagship, Hobart, 7000, Australia

Ocean acidification has been suggested to disturb fish behavioural responses to chemosensory cues. Most experiments have investigated coral reef species, while the effects on species from other parts of the world are largely unknown. The methods used to quantify chemosensory behaviour in fish are variable and in need of standardisation.

Two-current choice flumes were constructed in a range of sizes to accommodate fish from 3 to 200 mm length. The flumes carry two parallel laminar water flows through an arena where the experimental animal can choose between the two flows, and the two flows can be manipulated (e.g. hypoxia, hypercapnia, prey/predatory cues). The methodology was validated using a range of flow, dye and pilot testing. To eliminate bias in behavioural observation we used automated video analysis.

Stable laminar flow can be difficult to maintain and can be disrupted by deviations in flow. Flow controllers, baffles and multiple layers of honeycomb collimators are vital components. Long observation times are needed to quantify side preference. Subconscious biases make objective observation difficult and blinded observation or automated video analysis is therefore needed.

Using the flumes we show that predator avoidance was high in both control and high CO2 (1000 μatm) exposed Atlantic cod. Furthermore, Atlantic cod strongly avoided high CO2 water, even after one month of acclimation to high CO2. In goldsinny wrasse, the predator avoidance was slightly reduced by high CO2 exposure compared to control.

We present a reliable flume methodology for measurements of chemosensory behaviour that provides stable laminar flow and unbiased behavioural quantification. We show that high CO2 appears to have limited effects on temperate fishes. We encourage the use of these approaches in all future studies to enable a comprehensive and robust understanding of any CO2 effects on the chemosensory behaviour of fish.

16. The impact of angel’s wing on pteropod population in the Gulf of Naples (Western Mediterranean)

Sergio d’Albero (1,2,3)*, Paola Rumolo (2), Angelo Bonanno (2), Enrico Dinelli (3), Clara Manno (1)

1 BAS (British Antarctic Survey), Cambridge, Cambridgeshire, CB30ET, UK
2 IAMC-CNR, Napoli, Campania, Calata Porta di Massa, 80133, Italy
3 University of Bologna, Dep. Of Marine Biology, Emilia Romagna, 48123, Italy

Thecosomate Pteropods are particularly vulnerable to Ocean Acidification since their shells are made by of aragonite, a highly soluble form of biogenic carbonate in sea water. Marine areas with naturally high levels of carbon dioxide in the water provide a natural laboratory to study the adaptation strategy of calcifying organisms exposed to chronic low pH level. The Naples of Bay (Western Mediterranean) is a notable case where the presence of CO2 vents was already documented by local fishermans in the 70’s when they described the phenomenon of bubbles coming out from the sea surface as “the Wing of the Angel”. Despite several studies investigated the impact of the CO2 vents on calcifying benthic compartment, the effect on pelagic calcifying community, such as pteropods, is still poor understood.

Thecosomate Pteropods were collected during a cruise in two regions characterised by similar hydrological and biological regime but different carbonate chemistry regime (with and without the presence of CO2 vents). To understand the impact of high pCO2 -low pH levels on the pteropod population, the variability in biodiversity, abundance and shell quality of pteropods between the two regions were investigated. Shell morphology, dissolution and repair were examined using scanning electron microscopy.

Pteropod abundance and biodiversity were higher in the control than the CO2 vents stations. In all the stations the dominant pteropod was C. conica. We observed a difference in shell degradation of C. conica where in CO2 vent stations this pteropod presented higher shell dissolution and lower shell weight than those collected in the control stations. Moreover C. conica found at CO2 vent stations were smaller than those found in control conditions.

We suggest that C. conica could develop physiological and morphological change to counteract the higher energy demand due to the presence of chronic low pH exposition.

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.