Warming and Ocean Acidification in the Arctic Ocean Strongly Affect Ecosystem Balance

1. Key Points of the Announcement

• We clarified that the growth rate of phytoplankton in the Arctic Ocean in response to warming shows a much higher sensitivity than previously established theoretical models. In contrast, it was also found that the grazing pressure by microzooplankton—traditionally thought to be more temperature-sensitive than phytoplankton growth—does not exceed phytoplankton growth under natural environmental conditions because it depends on the availability of food.
• Under the influence of ocean acidification caused by increasing carbon dioxide levels, the growth of large phytoplankton tended to be suppressed, whereas the growth of small phytoplankton tended to accelerate.
• The interaction between warming and ocean acidification in the Arctic Ocean may lead to an ecosystem structure in which smaller phytoplankton become more dominant. This could result in lower production efficiency at higher trophic levels.

2. Overview

Koji Sugie, Researcher at the Research Center for the Earth Surface System, Research Institute for Global Change, Japan Agency for Marine-Earth Science and Technology (JAMSTEC; President: Hiroyuki Yamato), in collaboration with Dr. Bingzhang Chen, Senior Lecturer at the University of Strathclyde; Dr. Shigeto Nishino, Senior Researcher at the Arctic Research Center, JAMSTEC; and Associate Professor Toru Hirawake (currently Professor at the National Institute of Polar Research, Research Organization of Information and Systems; formerly at the Faculty of Fisheries Sciences, Hokkaido University), investigated the effects of environmental change on plankton communities in the Arctic Ocean.

During cruises of the JAMSTEC research vessel Mirai in 2017 and the Hokkaido University training vessel Oshoro Maru in 2018, plankton communities were sampled from the Arctic Ocean (Figure 1), and onboard incubation experiments manipulating temperature and carbon dioxide (CO₂) were conducted. As a result, we found that warming accelerated phytoplankton growth rates which were on average by 8.8 and 4.7 times faster for large phytoplankton (≥10 µm) and for smaller phytoplankton, respectively as compared with conventional theory. It was also notable finding that increased carbon dioxide concentrations suppressed the growth of large phytoplankton while accelerating the growth of smaller phytoplankton.

The grazing rates of microzooplankton rarely exceeded the growth rates of phytoplankton and showed a correlation with phytoplankton growth. While previous laboratory-based theories suggested that zooplankton have higher temperature sensitivity in metabolic rates than phytoplankton, the field results suggest that in natural environments, food availability is a limiting factor, indicating that zooplankton activity depends heavily on prey availability. Furthermore, it was found that rising CO₂ levels do not directly affect the grazing behavior of microzooplankton.

These findings suggest that although microzooplankton are relatively robust against environmental changes, the impacts on phytoplankton can lead to reduced production at higher trophic levels (Figure 2). The Arctic Ocean is undergoing some of the most dramatic environmental changes in the world, including sea ice retreat and warming. This study provides a theoretical understanding of how natural plankton communities respond to such changes and represents a significant advance in forecasting the present and future state of the rapidly changing Arctic ecosystem.

Figure 1. Sampling stations of experiments conducted in 2017 and 2018 research cruises.

Figure 2. Schematic diagram of an ecosystem pyramid based on phytoplankton of different sizes (left). This study suggests that future warming and ocean acidification may lead to a dominance of smaller phytoplankton, as shown on the right side of the left diagram, potentially resulting in a decline in higher trophic level organisms (top predators: TP). The right side shows microscope images of large and small phytoplankton, as well as microzooplankton.

This research will be published in Scientific Reports on August 20, (Japan Time). It was supported by the Arctic Challenge for Sustainability II (ArCS II: JPMXD1420318865), a project funded by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), and by the Grants-in-Aid for Scientific Research (KAKENHI Grant No. 15K21683).

3. Background

The Arctic Ocean is one of the regions most severely affected by global environmental change, with rising water temperatures and melting sea ice already underway. Understanding how such dramatic changes are impacting the ecosystem is an urgent challenge. The increase in atmospheric carbon dioxide (CO₂) not only raises sea surface temperatures through global warming but also causes ocean acidification, a process in which CO₂ dissolved in seawater shifts its weak alkalinity toward a more acidic state.

Our previous research (Sugie et al., 2020) showed that the interaction between warming and ocean acidification in the Arctic Ocean leads to an increased dominance of smaller phytoplankton within the community. However, that study left unresolved whether this shift in favor of smaller phytoplankton was due to changes in the prey itself or in its predators. The specific responses of different ecosystem components to environmental change remained unclear, leaving the underlying mechanisms of ecosystem transformation poorly understood.

Given the complexity and diversity of life in ecosystems, there is a tendency for conclusions to diverge. Therefore, to interpret ecosystem responses more systematically, it became necessary to develop a new experimental approach capable of evaluating the effects of environmental change on functionally distinct biological groups (e.g., plants vs. animals, large vs. small organisms). In situ experimental studies were also required using natural plankton assemblages.

4. Development of a New Experimental System

In this study, we applied a modified version of the two-point dilution method (Chen, 2015), which enables the separate analysis of phytoplankton growth rates and microzooplankton grazing rates. The experimental setup included four parallel treatments: (1) ambient water temperature (LT), (2) warming by +4°C (HT), (3) CO₂ addition at ambient temperature (LTHC), and (4) simultaneous warming and CO₂ addition (HTHC). This allowed us to assess the effects of each environmental factor on different functional groups of organisms. Furthermore, by separating plankton into two size classes—larger than and smaller than 10 µm—we developed an experimental system capable of evaluating how size composition (Figure 1), which has significant implications for higher trophic levels in the ecosystem, responds to environmental change.

5. Results

This study revealed that increasing CO₂ concentrations act as an inhibitory factor for the growth of large phytoplankton, while promoting the growth of smaller phytoplankton. Microzooplankton, on the other hand, were found to be largely unaffected directly by environmental changes, and instead were indirectly influenced through the dynamics of phytoplankton, which serve as their food and are directly affected by those changes. In other words, the trend observed in Sugie et al. (2020) can be attributed primarily to the response of phytoplankton to environmental change.

The mechanism is as follows:
Phytoplankton in the Arctic Ocean exhibited increased growth rates with rising seawater temperatures. Both large and small phytoplankton showed growth rate increases of approximately 0.1 d⁻¹ for each 1°C rise in temperature (Figure 3, top). Compared to conventional theories such as Q₁₀ or Eppley curve derived from laboratory experiments, this increase was on average 8.8 times higher for large phytoplankton (≥10 µm) and 4.7 times higher for smaller ones, indicating that Arctic phytoplankton are highly sensitive to temperature changes. This temperature-driven growth rate also varied with CO₂ levels. Growth in large phytoplankton decreased significantly with higher CO₂, whereas small phytoplankton showed a significant increase in growth (Figure 3, bottom). Although the average response to increased CO₂ ranged from −0.019 to +0.023 d⁻¹ per 100 µatm CO₂—less than the influence of temperature—it was clear that high CO₂ levels under warmer conditions suppressed growth in large phytoplankton while promoting growth in smaller ones. Thus, simultaneous increases in both temperature and CO₂ in the Arctic Ocean are likely to favor the survival of smaller phytoplankton over larger ones.

Figure 3. Change in the growth rate of phytoplankton against the change in temperature(upper panels) and CO₂(lower panels).

The grazing rates of microzooplankton also showed tendencies to vary with temperature and CO₂ concentration, similar to phytoplankton. This variation was considered to be driven by the correlation between phytoplankton growth rates and microzooplankton grazing rates. In particular, because the response of microzooplankton to elevated CO₂ concentration had remained unclear, we normalized the data based on phytoplankton growth rates to exclude their influence and extracted the effects of CO₂ for analysis. As a result, we revealed for the first time in the world that rising CO₂ concentrations do not directly affect the grazing pressure of microzooplankton (Figure 4). In other words, microzooplankton grazing pressure is governed by the growth of phytoplankton, which is influenced by environmental changes, indicating that environmental changes act as indirect drivers.

Figure 4. The ratio of phytoplankton growth rate-normailzed microzooplankton grazing rate between control and high CO₂ conditions. The mean values of the ratio did not differ from the unity indication no direct impact of CO₂ on grazing.

The adaptive capacity of microzooplankton to environmental change reflects the robustness of the ecosystem. However, when phytoplankton of different sizes respond differently to such changes, it can disrupt the ecosystem balance. In an ecological pyramid, each predator-prey interaction results in the loss of approximately 90% of energy due to metabolic processes. This means that ecosystems beginning with smaller phytoplankton, which require more trophic steps to reach top predators, transmit primary production less efficiently to higher trophic levels (Figure 1, left).

This study suggests that in the Arctic Ocean, ongoing warming driven by increased atmospheric CO₂ concentrations may reduce large phytoplankton populations while favoring smaller ones—ultimately leading to a decline in higher trophic-level organisms.

6. Future Outlook

The newly developed incubation method used in this study has enabled the evaluation of how functionally distinct components of an ecosystem respond to environmental change. Since the environmental factors of concern differ by ocean region, applying this method to various regions will allow for a better understanding of ecosystem functions and how they are altered.

Ecosystem studies often suffer from diverging conclusions due to the high diversity of species and functions involved. However, as demonstrated in this study, approaching ecosystems by focusing on functional roles and interpreting responses theoretically is critically important. Moving forward, we aim to apply this experimental approach to other marine regions beyond the Arctic Ocean. By constructing theories of ecosystem behavior based on real-world environmental data, we hope to simplify and mathematically model the complexity of marine ecosystems, ultimately contributing to more advanced simulations and future projections.