The next challenge: how do multiple environmental drivers influence ocean biota?

Introduction
The summer OCB meeting in July 2012 featured for the first time a special session on “Multiple stressors in marine ecosystems” that was chaired by Cindy Lee (SUNY Stony Brook). The five speakers of this timely session – Jorge Sarmiento (Princeton Univ.), Lisa Levin (Scripps Inst. of Oceanography), Wei-Jun Cai (Univ. of Delaware), Nicolas Gruber (ETH Zurich), and Philip Boyd (NIWA New Zealand) – provided an illustrative range of approaches and viewpoints, in both their presentation and in a panel discussion, on this fledgling research field. In research fields such as ocean acidification, there has been a growing appreciation that restricting environmental perturbation experiments solely to manipulation of CO2/pH can only fill in part of the puzzle that encompasses the complex responses of ocean biota to climate change (Boyd, 2011). The recent Ocean in a High-CO2 World meeting provided some interesting statistics on how researchers are designing ever more complex environmental perturbation experiments (see article by Sarah Cooley, OCB News, Fall 2012). There has also been a growing focus on how concurrent changes in multiple oceanic properties will alter ocean biota, with special sessions at workshops run by intergovernmental organisations such as the North Pacific Marine Science Organization (PICES) and international programmes such as Integrated Marine Biogeochemical and Ecosystem Research (IMBER).

At the OCB Summer 2012 meeting, Philip Boyd updated the community about some prior and forthcoming activities associated with the emerging theme of multiple environmental drivers and ocean biota. Ocean global change researchers now increasingly appreciate that in addition to acidification, marine organisms will face simultaneous changes in temperature, oxygen, salinity, light, nutrients, and micronutrients, along with interactions among these drivers (Fig. 1). Here, we provide a summary of several recent thematic issues of journals on the effects of a changing ocean on its biota, and also publicize the first dedicated meeting on this topic that will take place in mid-2014. We conclude by discussing some of the
challenges that lie ahead in developing this research topic.
In late 2012, the journal Marine Ecology Progress Series (MEPS) published an open access theme section on “Biological responses in an anthropogenically modified ocean” (Boyd and Hutchins, 2012), that comprised seven papers and an Introduction to the theme section. These contributions focused on a wide range of topics from the response of the ocean’s biological pump to a changing ocean (Passow and Carlson, 2012) to the range of environmental controls on calcifying coccolithophores (Raven and Crawfurd, 2012). Other research presented ranged from phytoplankton functional traits to the responses of harmful algal blooms to changing oceanic conditions. In 2013, the journal Evolution will publish a special section (edited by Daphne Fairbairn and Sinead Collins) that brings together a set of papers focused on the potent linkages between experimental evolutionary biology and the biota in aquatic systems. These contributions provide valuable insights into the role that experimental evolutionary biology can play in helping to understand the responses of ocean biota to changing environmental conditions, as recently reported by Lohbeck et al. (2012). Some of the contributions of this
special section are already available online as advanced publications, such as the Introduction to the section by Reusch and Boyd (2013). Understanding the adaptive responses of marine organisms to selection by climate change will also be the topic of a session at the upcoming 2013 OCB summer meeting (co-organized by T. Rynearson and D. Hutchins).

Terminology – stressors or drivers?
In the Introduction to the MEPS theme section, Boyd and Hutchins (2012) reappraise the rich literature on the topic of environmental stressors from the freshwater and ecotoxicology literature. They point out that although the term “multiple
stressors” has been widely used in these canons, as the focus has often been on the detrimental effects of pollutants, it is not always the best term to use when discussing environmental change in the marine environment. They put forward a case that changing oceanic conditions will result in both detrimental effects for some groups or species (the “losers”) and beneficial effects for others (the so-called “winners”). For example, warming has been suggested to favour nanoflagellates relative to diatoms, while higher dissolved carbon dioxide concentrations may be disadvantageous to coccolithophores, and at the same time benefit nitrogen- fixers (Fig. 2). Thus, the generic term ”driver” is a broader and often more accurate descriptor than stressor when discussing the general effects of global anthropogenic change on ocean biota. A glance through the prior literature also revealed that the potential interactive effects of multiple drivers – the so called synergisms and antagonisms – on the biota had been poorly defined. To redress this, Boyd and Hutchins provide a list of revised definitions in their Introduction, and stressed the need to more rigorously contextualise the use of such definitions in publications. For example, they point out that synergisms and antagonisms each require a further qualifier to detail whether they are describing negative or positive effects for the organism. Synergisms and antagonisms can be used to refer to initial interactions between environmental drivers that subsequently affect the biota, or to interactive effects on the biota that result in a direct biological consequence.

An ecosystem level approach
Another key issue that is addressed in their Introduction to the MEPS theme section is the effects of multiple drivers across different trophic levels. For example, phytoplankton at the base of the food web may be influenced by changes in up to six different drivers (light, pH, CO2, temperature, nutrient and trace metal supply, and their interplay), whereas higher trophic levels will be directly influenced by fewer oceanic properties. There is also the important issue of differential susceptibility to a changing ocean and its potential to restructure food webs. Boyd and Hutchins (2012) note that much of the ongoing research on multiple environmental drivers and ocean biota is on primary producers, but effects of changing oceanic conditions on higher trophic levels could be equally influential in reshaping ecosystems and their functioning. At higher trophic levels, there are also the potentially confounding effects of the interplay of ‘bottom up’ environmental and ‘top down’ ecological controls, along with other ‘top-down’ anthropogenic pressures such as harvesting (Fig. 3). Several recent reviews have also raised some of these issues (Brose et al. 2012; Caron and Hutchins, 2012).

The challenge
The study of the effects of multiple drivers on ocean biota represents a major step up in complexity of virtually all facets of research relative to that encountered when investigating a sole driver such iron supply or ocean acidification (Table 1). Such issues will also become increasingly evident as the scientific community attempts to communicate the findings of such studies to policymakers. There is much to be learned from the rapid progress made by the ocean acidification community (Boyd, 2011). Central challenges in the coming years include building a research community and developing methodologies to conduct complex multivariate experiments. Equally important will be engaging research and government agencies, and informing them of the need to directly tackle the issue of how multiple environmental drivers will alter the ocean’s ecosystems and biogeochemistry in the coming decades. In order to help set up a forum to specifically address some of the above issues, members of the OCB community have been actively seeking a suitable workshop for a dedicated meeting. In 2012, David Hutchins (USC), Adina Paytan (UCSC), Shannon Meseck (NOAA), and Philip Boyd (NIWA) submitted a successful application for a new Gordon Research Conference (GRC) to be broadly focused on how the full spectrum of drivers in the changing ocean will affect all levels of marine food webs. This first Ocean Global Change Biology GRC will take place July 6-11, 2014 at the Waterville Valley Resort (Waterville Valley, NH, Chair D.A. Hutchins). We hope to entrain strong interest and participation by the OCB community at this meeting, as we begin to plan strategies to meet the next challenge thrown at us by global climate change.

References
Boyd, PW., 2011, Nature Geoscience 4, 1-2.
Boyd, P.W., C.S. Law, 2011, NIWA information series # 79, ISSN 1174- 264X.
Boyd, P.W., D.A. Hutchins, 2012, Marine Ecol. Prog. Ser. 470,123-290.
Brose U. et al., 2012, Phil. Trans. R. Soc. B 367, 2903–2912.
Caron, D. A., D. A. Hutchins, 2012, J. Plank. Res., doi:10.1093/plankt/fbs091.
Fu, F.-X. et al., 2008, Limnol. Oceanog. 53(6): 2472- 2484.
Griffith, G.P, E.A. Fulton, A.J. Richardson, 2011, Glob. Change Biol., doi: 10.1111/j.1365-2486.2011.02453.x.
Hare, C. E. et al., 2007, Deep-Sea Res. I 54, 732-746.
Hutchins, D. A. et al., 2007, Limnol. Oceanog. 52, 1293-1304.
Lohbeck, K.T., U. Riebesell, T.B.H. Reusch, 2012, Nature Geosci. 5, 917- 917 doi:10.1038/ngeo1637.
Passow U., C.A.Carlson, 2012, Marine Ecol. Prog. Ser. 470, 249-271.
Raven J.A., K. Crawfurd, 2012, Marine Ecol. Prog. Ser. 470, 137-166.
Riebesell, U. et al., 2000, Nature 407, 364–367.
Reusch, T.B.H., P.W. Boyd, 2013, Evolution, DOI: 10.1111/evo.12035.

Boyd P. W. & Hutchins D. A., 2013. The next challenge: how do multiple environmental drivers influence ocean biota? Ocean Carbon & Biogeochemistry News 6(1): 1-4, Winter 2013. Article.


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