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Issue n°24 - August 2013

Issue n°24 - August 2013
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In this issue

Lisa Maddison

IMBER International Project Office, Bergen, Norway

In January this year, IMBER held its third biennial IMBIZO (the Zulu word for 'a gathering') at the National Institute of Oceanography in Goa, India.

The theme of IMBIZO lll was The future of marine biogeochemistry, ecosystems and societies. This brought scientists from different disciplines together to explore the complex and inextricably linked interactions between humans and the oceans. The proven format of three concurrent but interacting workshops was followed, to consider multi-dimensional approaches to the challenges of global change in continental margins, open ocean systems and dependent human societies.

Workshop 1 focused on biogeochemistry-ecosystem interactions in changing continental margins. The presentations covered margins from polar to tropical regions and also oxygen minimum zones. Some regions, like Arctic shelves, are strongly impacted by global warming, with projected declines in productivity and CO2 uptake capacities. Others are subjected to multiple stressors directly related to human activities.

The functioning of the microbial carbon pump (MCP) at molecular to food web scales and its vulnerability to human perturbations was the subject of workshop 2. Participants agreed that its pivotal role in determining food web structure allows relatively minor anthropogenic or climatic perturbations to potentially cause major shifts in the ocean’s role in sequestering carbon and thus in regulating the climate.

The complex human-ocean-human interactions, drivers and pressures, with respect to global change was the focus of the third workshop. Presentations looked at the vulnerability and adaptation of marine-dependent communities to global change and the governance responses to assessing and mitigating the impacts.

The first seven articles in this issue showcase some of the papers that were presented at each of these workshops. I hope that you will enjoy reading these. They will remind those who were there about the scientific discussions and interactions. And for those who were not lucky enough to attend, it will provide an idea of the level of scientific excellence that we hope will encourage you to attend IMBIZO lV in 2015!

IMBIZO lll was funded as a EUR-OCEANS conference and we also received generous support from CSIR-NIO, SCOR, PICES, NASA and UBO. I would also like to take this opportunity to thank all our local hosts at NIO - especially the Director, Dr. Wajih Naqvi, Damodar (Damu) Shenoy and Siby Kurian. Without your generosity, dedication and enthusiasm, IMBIZO lll would not have been the success that it was.

Also in this issue you can also read about a brand new joint IMBER-CLIVAR initiative that aims to investigate marine biophysical interactions and the dynamics of upwelling systems.

IMBER has recently endorsed three new research projects, and we report on the achievements of the Population Outbreak of Marine Life (POMAL) project.


IMBIZO III group photo
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Science highlights from IMBIZO III

Continental Margins

Oxygen minimum zones, zooplankton layers, and global change

Karen Wishner

University of Rhode Island, Narragansett RI 02882, USA


The National Insitute of Oceanography in Goa, India, close to shores of the Arabian Sea, was the perfect location to inspire reflections on processes in oceanic oxygen minimum zones (OMZs). The friendly hosts of the IMBIZO III meeting, especially the Director, Dr. Wajih Naqvi, and the many other local faculty and students who work on and think about OMZs, created a vibrant intellectual (and gastronomic) setting to delve into current and future OMZ issues and comparisons with coastal hypoxia. 

OMZ regions are some of the most extreme oceanic habitats, with oxygen concentration in their core depths near the limits of aerobic life (Seibel 2011). Yet just above those depths are large animal populations, including important fisheries resources for many nations. Significant OMZs are located in the Arabian Sea, Eastern Tropical Pacific and off Namibia, and their effects influence the coastal ecology and economic resources of the adjacent nations. OMZs are expected to expand in geographic and vertical extent with increased global warming, with many potential biological and economic consequences (Stramma et al. 2010).

Through previous participation in the JGOFS Arabian Sea Program, and over two decades working in the Eastern Tropical North Pacific, we have helped elucidate some of the broad principles structuring zooplankton distributions in these extremely hypoxic environments. It has been known for many years that resident zooplankton biomass and abundance in the OMZ core (depth zone of lowest oxygen) are much reduced compared to more oxygenated regions (e.g. Wishner et al. 1998, 2008; Smith and Madupratap 2005)  (Fig. 1), although substantial diel vertical migration occurs several hundred meters into depths of very hypoxic water. 


Figure 1. Photographs of fresh zooplankton samples from MOCNESS net tows in the Eastern Tropical North Pacific. Left: a sample from the OMZ core (400-450 m). Right: a sample from the lower oxycline zooplankton layer just below the OMZ core (600-625 m).


What is not as well appreciated is that both the upper and lower oxyclines (oxygen gradients) at the upper and lower OMZ core boundaries are locations of strong zooplankton and fish layering. Several investigators have studied the layers associated with the upper boundary of the oceanic OMZ, which has strong oxygen and temperature gradients. However, another less well known zooplankton and micronekton layer exists at the lower oxycline of the OMZ at mesopelagic depths (Wishner et al., 1995, 2008). We have found that this represents an order of magnitude increase in zooplankton biomass over a small depth interval and occurs at a very precise oxygen concentration (Wishner et al. in review). The animals in this layer (copepods, fish, shrimp) are important in the processing of sinking material as part of the biological pump and also in trophic webs of the deeper ocean. The lower oxycline zooplankton layer may also be essential in benthic-pelagic coupling on continental slopes, since it is a potential food source for benthic animals where the OMZ intersects the sea floor (Wishner et al. 1995, Levin 2003). 

If the depths of these layers shift as a result of future OMZ expansion, zooplankton distributions and their feeding relationships with fish and benthos may be altered. For example, as the upper oxycline boundary oscillates vertically in time and space, including possible long-term shifts associated with OMZ expansion, zooplankton and fish layers will shift depth also. These layers are the prey of larger commercial fish, and the diving and feeding behaviour of those fish may be affected (Koslow et al. 2011, Stramma et al. 2011). At the lower oxycline, zooplankton layers may be forced deeper below an expanded OMZ, with potential impacts on vertical fluxes and both pelagic and benthic food webs (Wishner et al. submitted). Scientists and policymakers must begin to evaluate and plan for possible long-term ecosystem and economic consequences of these changing OMZ boundary layers.


  • Koslow, J.A., Goericke, R., Lara-Lopez, A., Watson, W., 2011. Impact of declining intermediate-water oxygen on deepwater fishes in the California Current. Mar. Ecol. Prog. Ser. 436: 207-218.
  • Levin, L.A., 2003. Oxygen minimum zone benthos: Adaptation and community response to hypoxia. Oceanogr. Mar. Biol. 41: 1-45.
  • Seibel, B. A.,  2011. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J. Exper. Biol.  214: 326-336.
  • Smith, S. Madhupratap, M., 2005. Mesozooplankton of the Arabian Sea: Patterns influenced by seasons, upwelling, and oxygen concentrations. Prog. Oceanogr. 65: 214-239.
  • Stramma, L. Schmidtko, S., Levin, L.A., Johnson, G.C., 2010. Ocean oxygen minima expansions and their biological impacts. Deep-Sea Res. I 57: 587-595.
  • Stramma, L., Prince, E.D., Schmidtko, S., Luo, J., Hoolihan, J.P., Visbeck, M., Wallace, D.W.R., Brandt, P., Körtzinger, A., 2011. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nature Climate Change 2: 33-37. 
  • Wishner, K.F., Ashjian, C.J., Gelfman, C., Gowing, M.M., Kann, L., Levin, L.A., Mullineaux, L.S., Saltzman, J., 1995. Pelagic and benthic ecology of the lower interface of the eastern tropical Pacific oxygen minimum zone. Deep-Sea Res. I. 42: 93-115.
  • Wishner, K.F., Gowing, M.M., Gelfman, C., 1998. Mesozooplankton biomass in the upper 1000 m in the Arabian Sea: overall seasonal and geographic patterns, and relationship to oxygen gradients. Deep-Sea Res. II. 45: 2405-2432.
  • Wishner, K.F., Gelfman, C., Gowing, M.M., Outram, D.M., Rapien, M., Williams, R.L., 2008. Vertical zonation and distributions of calanoid copepods through the lower oxycline of the Arabian Sea oxygen minimum zone. Prog. Oceanogr. 78: 163-191.
  • Wishner, K.F., Outram, D.M., Seibel, B.A., Daly, K.L., Williams, R.L. Zooplankton in the Eastern Tropical North Pacific: Boundary effects of oxygen minimum zone expansion. Deep-Sea Res. I (in press).
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The productivity of the Arctic Ocean of the future

Paul Wassmann

Institute of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and economy, University of Tromsø, N-9037 Tromsø, Norway


No region on our planet is subjected to stronger climate change than the Arctic Ocean. The average atmospheric temperature of the entire Arctic region has increased 2-3 times more compared to the global average. The extent of the ice cover has decreased about 10% per decade, and loss rates since 2000 are even higher, with record shrinkage in 2007 and 2012. There is speculation as to when the central Arctic Ocean will loose its summer ice cover, with estimates ranging from within a few years, to 1-2 decades from now. Meanwhile, ice thickness has also decreased significantly: > 70% of the ice volume has been lost in the past few decades. As a result, the Arctic Ocean receives more light, contains more fresh water, has much thinner and variable ice cover, and its surface is much darker so that it now warms up more quickly. What do these changes, which are the most significant climatological and ecological alterations experienced by any of our oceans, mean for the base of life - marine productivity?

Primary production is the production of organic compounds from atmospheric or aquatic carbon dioxide. It is distinguished as either gross primary production or harvestable production, the latter designating the amount of organic compounds that can be extracted, or harvested, from ecoregions. Why should we care about the current and future productivity in the Arctic Ocean? 

1. Some of the world’s largest fisheries are located at the southern perimeter of the Arctic Ocean. These have shown a tendency to move northwards because of the impact of global warming that initially results in shrinkage (and thinning) of summer sea ice. These fisheries have a significant economic bearing for all Arctic nations, including indigenous people of the region. 

2. The Arctic Ocean is considered to be one of the last pristine regions of the world, and climate change may alter this and reduce its biodiversity. What level and type of biodiversity losses are expected?

3. The Arctic Ocean functions as a major draw-down of atmospheric CO2, but climate change and primary production (and respiration) could alter the ecoregion into one that releases CO2 to the atmosphere, thus accelerating the ever-increasing concentrations of greenhouse gases. How significant will this increase be?

4. The atmospheric transport of contaminants from equatorial regions towards the Arctic Ocean is significant. Algae and small marine animals bio-accumulate contaminants, amplifying their concentration, which could result in a food security risk for both indigenous and non-indigenous consumers. How much will the livelihoods of consumers be put at risk?

The primary production of the Arctic Ocean, which has a circular current pattern that is closely connected to two adjacent oceans, is strongly influenced by the advection of nutrient-rich waters. The thinning and rapid shrinking of the ice in summer could result in a significant increase in primary production in previously ice-covered waters. However, the resulting strong stratification and warming of the surface water, together with the low nutrient concentrations of the deep Arctic Ocean surface waters, prevent primary production from reaching very high levels. The smaller organisms that occur in a freshening ocean, and the increase in respiration caused by warming, result in less food and smaller prey, which can have negative ramifications for fish, seals and whales.


Models of current and future climatic conditions have been applied to estimate primary production in the Arctic Ocean. In the sub-Arctic northeastern North Atlantic, primary production will decrease significantly - by 20-40% towards the end of the century - as a result of surface water warming. This decrease in the food available for fish could have major ramifications on one of the world’s most significant fisheries. In the currently ice-covered low-productivity waters of the Barents Sea, primary production will increase, particularly in the northeast. This may support a future increase in the fishery. There will be a clear increase in primary production, by > 50%, along the entire continental shelf adjacent to the low-productive, deep Arctic Ocean. It could be that a significant proportion of the fisheries will be found here towards the end of the century. Russia will benefit from these changes, but Norway will possibly be faced with reduced fish food production and consequently a reduced fishery, except north of Svalbard.

It is therefore extremely important that we give careful consideration to the primary production of the future. It could have major ramification for fisheries, the cycling of climate gases and also for the contamination of seafood.

Figure 2 (courtesy of Dag Slagstad, SINTEF, Trondheim, Norway) shows the average primary production of the Arctic Ocean and adjacent North Atlantic (scale: g C m-2 year-1) for the period 2051-2060. The IPCC climate change scenario A1 (implying a global atmospheric temperature increase of + 3.8oC in 2100) was applied. According to the model, ice cover still prevents major increases in primary production in the central Arctic Ocean, but an increase along its perimeter is visible/observed. However, most current ice models are unable to mimic today’s ice reduction, let alone predict future development. Primary production will support a potential future fishery along the Arctic Ocean shelves and shelf breaks. Whether commercially important fish will extend so far north and into the very cold water there, remains to be seen.


Figure 2. The average primary production of the Arctic Ocean and adjacent North Atlantic (scale: g C m-2 year-1) for the period 2051-2060

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Open Ocean

Processes and mechanisms of microbial carbon sequestration in the ocean (Introduction to a national Chinese research project)

Nianzhi Jiao1, Chuanlun Zhang2, Chao Li3, Xiaoxue Wang4, Hongyue Dang1, Rui Zhang1, Yao Zhang1, Kai Tang1, Zilian Zhang1, Dapeng Xu1

1 Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen 361005 China

2 State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, China

3State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China

4Key Laboratory of Marine Bio-Resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China.



The ocean is the largest carbon sink on the earth. The well-known biological mechanism for carbon sequestration in the ocean is the biological pump (BP), which is driven by primary production in the euphotic zone and then mediated by the sinking process of particulate organic carbon (POC) in the water column. However, the POC that reaches the sea floor is only a tiny fraction of the total primary production, with the majority of POC being respired as CO2 or converted into dissolved organic carbon (DOC) in the water column. The DOC pool is huge, and accounts for more than 90% of the total marine organic carbon, which is equivalent, in amount of carbon, to the total inventory of atmospheric CO2. Furthermore, the majority of marine DOC is recalcitrant, which has an average residence time of ~5000 years and thus plays an important role in the sequestration of carbon in the ocean. However, the mechanisms controlling the generation and removal of the recalcitrant DOC (RDOC) are largely unknown. A recently proposed concept, the microbial carbon pump (MCP) (Jiao et al., 2010) offers a formalized and mechanistic focus on the significance of microbial processes in carbon storage in the RDOC reservoir, and a framework for testing the sources and sinks of DOC and the underlying mechanisms. Understanding of the functioning and efficiency of the MCP is urgently needed, as ocean warming may change carbon flux partitioning between the BP and the MCP, potentially favouring the MCP.

A Scientific Committee on Oceanic Research (SCOR) working group (http://ime.xmu.edu.cn/mcp/; or www.scor-int.org /WorkingGroups /wg134.htm), comprising 26 scientists from 12 countries, was formed in 2008 to address this multi-faceted biogeochemical issue relating to ocean carbon cycling and global climate change. A major national project on the MCP was launched by the Ministry of Science and Technology of China in 2013 (No. 2013CB955700), to delineate the key processes and mechanisms of the MCP at molecular, ecological and biogeochemical process levels, as well as to evaluate the environmental consequences of the MCP at current and geological time scales. This project will address the active and passive pathways of RDOC production through the MCP, molecular and environmental regulatory mechanisms of the RDOC production, dynamics of the MCP along environmental gradients, evidence for carbon sequestration by the MCP in ancient and modern oceans, as well as potential MCP applications for carbon sink.

Features of the MCP


Figure 3: Diagram of the microbial carbon pump (in yellow) and relevant biological processes involved in carbon cycle in the ocean (Jiao et al., 2010).

The MCP does not rely on POC sinking, it emphasizes the microbial transformation of DOC from labile to recalcitrant states, and is concerned with both microbial uptake and excretion of DOC compounds. The MCP is a distinct concept from the well-known “microbial loop” that refers to the microbial processes of picking up DOC from the water, forming POC, and transporting the carbon to upper trophic levels. The MCP also implies that “carbon fixation” does not equal “carbon storage” and an ecosystem with “high primary production” does not necessarily have large carbon storage capacity. The MCP is influenced by chemical conditions (such as nutrients, organic matter, etc.) instead of physical processes (such as sinking, mixing, etc.), and is impervious to the effects of depth.

The overall objectives

Through interdisciplinary exchange between biologists, chemists and geologists, and comparative studies between ancient and modern marine environments, the project will put the MCP theoretical framework into practical field and laboratory studies. These will include elucidating the MCP processes and mechanisms, assessing the potentials of carbon storage in Chinese coastal waters, and establishing scenario models for marine DOC dynamics under global warming. We hope to provide a new, integrated view of microbial mediated carbon flow in the marine environment to fill knowledge gaps in oceanic carbon sequestration.

The cornerstone themes

The MCP project consists of four scientific themes that will work independently, and also across themes to better understand this innovative carbon sequestration mechanism: the active and passive pathways of the RDOC production through the MCP; molecular and environmental regulatory mechanisms of RDOC production; dynamics of the MCP across environmental gradients; and evidence for carbon sequestration by the MCP in the ancient oceans. Each will address basic scientific questions, and thus, the results can be used to evaluate the potential of MCP approaches to carbon sequestration in the ocean, and to provide government officials with needed data, insight, tools and indicators for making future environmental and climate polices.

The active and passive pathways of the RDOC production through the MCP

1) The active process

This sub-project targets the generation of extracellular metabolites (RDOC-like compounds) such as D-amino acids and exopolysaccharides produced by marine microbes. Integration of chemical composition assessments with microbiological analyses could provide novel views on the interactions and processes that govern microbial metabolism in the ocean. The analysis of specific genomic features will be combined to gain insight into microbe-molecule interactions, and the use of pure cultures to study the interaction of genes and the chemical structure of the molecules. We plan to: (i) begin with the interaction between the microbial cell wall/membrane and the external environments, and then study the substrate (labile DOC) specificity of the transporters and the distribution/ function of the transporter proteins in different marine environments; (ii) probe the cell metabolic pathways for biomass synthesis or energy production that could modify the chemical structure of substrates and potentially change the labile/refractory nature of the DOC, including acylation of polysaccharides and biosynthesis of D-amino acids by racemases with L-enantiomers as substrates; (iii) explore the molecular basis of release of microbial extracellular polymeric substances (EPS) and the chemical composition of EPS; (iv) estimate the contribution of the RDOC-like compounds to marine carbon storage. 

2) The passive process

This sub-project will address the ecological characteristics (abundance, production, diversity, etc.) of viruses and bacteria in typical marine environments of the South China Sea and the western Pacific Ocean. Marine viruses are the most abundant biological entities in the ocean, (average concentration of 3×109 particles/L), and play an important role in marine ecosystem and biogeochemical cycling. In the marine environment, the ecological function of viruses is achieved by infection and lysis of their hosts. The effect of viruses on host abundance, production, diversity and community structure will affect the flow of material and energy in marine food webs. Unlike predation, viral lysis drives carbon and nutrients back to the dissolved form, which can then be used again by bacteria and other organisms. This cycling is known as the “viral shunt”. Changes of the direction of organic matter will significantly affect carbon cycles in the ocean; some DOC produced by viral lysis will no longer be utilized by other microbes and will remain in the water as RDOC for a long period of time. In this study, the lysis process, as well as environmental factors affecting lysis, will be analyzed using incubation experiments. The analysis of the chemical composition and bioavailability of DOC released by viral lysis will provide a comprehensive understanding of virus-related carbon sequestration and, therefore, carbon cycles in the ocean.  

3) The effect of grazing

This sub-project will examine the distribution and ecological function of protozoan grazers in ocean gradient environments. We will characterize the products of grazing activity, i.e., the composition and quantity of released DOC (including RDOC) using both in situ incubation and lab culture experiments. 

Previous studies have shown that heterotrophic bacteria can process and reprocess some of the DOC and about half of the oceanic primary production is channeled via bacteria into the microbial loop. In aquatic systems, protozoa (mainly ciliates and heterotrophic flagellates) are the major consumers of bacteria and the pico-sized phototrophic eukaryotes. Considering the great abundance and biomass of phytoplankton and bacteria, it is reasonable to believe that the grazing activity of protozoa plays an important role in the production and cycling of DOC (including RDOC) in the ocean. However, previous studies focused more on the quantity of DOC production during grazing activity, not the quality of the molecular composition of the DOC. This will help us to reveal the role of protozoan grazing in the production/accumulation of RDOC in the modern ocean.

Molecular and environmental regulatory mechanisms of RDOC production

At the molecular level, the MCP is concerned with both microbial uptake and output of DOC, covering a wide range of levels from genes to ecosystems. Transporter proteins allow Gram-negative bacteria to take up scarce resources from nutrient-limiting environments. POC and DOC are dominated by high-molecular-weight (HMW) compounds. The HMW DOC needs to be hydrolyzed into smaller molecules by extracellular enzymes to allow transport across the outer membrane. Thus, genes associated with cross-membrane transportation and extracellular hydrolysis are critical for building DOC molecules appropriate for microbial assimilation. It is important to examine the microbial, genetic and enzyme repertoire for these genes. This can be done using (meta-) genomic and (meta-) transcriptomic analyses. The focus at the molecular level will be on microbial transporters and enzymes that have a pivotal role in cleaving, decomposing, taking up and transforming DOC (such as peptidoglycan and extracellular polymeric substances).



Microbial processing of carbon in sea water/MCP is also regulated by environmental factors, e.g. nutrients and organic matter derived from land. Compared to the biological pump, which is inefficient in regions of insufficient water depth, such as estuaries, the MCP is influenced by intrinsic biological mechanisms and their environment, such as chemical conditions - its efficiency is determined by the nutrients in the water. When nutrients are replete, both ammonium and nitrate can be used by heterotrophic bacteria with nitrate reductase genes that are induced by ambient nitrogen availability. Currently, we are studying whether enhanced terrestrial input of nutrients will mobilize DOC for microbial respiration, thus potentially influencing MCP carbon sequestration efficiency. We hope that this research will provide an unconventional reasoning, that by reducing the use of fertilizer and preventing pollution into coastal waters, we could boost the efficiency of the oceanic carbon sink. This possibility deserves further investigation, not only for science but also for policy.

Dynamics of the MCP across environmental gradients 

This sub-project will investigate the dynamic capacity of the MCP for carbon storage along environmental gradients. The focus is a comparison of the BP and the MCP, including the efficiency of the BP, possible mechanisms of the MCP and their relationship to different environmental factors. We previously compared the BP with the MCP in marine upwelling areas, and results revealed that many upwelling regions are actually sources rather than sinks of CO2, although upwelling areas are known to be productive in carbon fixation. When nutrient-rich deep water upwells to the upper ocean, enhanced nutrient input and accumulated labial organic carbon could stimulate microbial respiration, exacerbating the attenuation of POC export and influencing a region to be a carbon sink or source.

Microbial lipids will be used to reflect changes in the community structure, the difference in organic substrates and changes in environmental conditions (Table 1).  The advantage of carbon or hydrogen isotope analysis of lipid biomarkers is to investigate carbon metabolism or carbon flow at the molecular level. The isotope fractionation of an organism is determined by the autotrophy (carbon dioxide fixation) or heterotrophy (organic degradation) processes. Isotope fractionations differ according to differences in carbon or energy metabolism. In this project, carbon and hydrogen isotopes will be used on environmental samples as well as major culture strains, including E. coli, Psedomonas, which are type strains of biological membranes, and aerobic anoxygenic phototrophic bacteria (AAPB), which are type strains of RDOC production. Other strains with special carbon and energy metabolism will also be investigated. Because viruses may affect the carbon or hydrogen metabolism of the host,  isotope fractionation will be compared with or without the presence of viruses.

Table 1. Organic proxies relevant to the production and transformation of the recalcitrant dissolve organic carbon.

Indices Application References
BIT, lignin, long-chain alkane Terrigenous materials input in marine environment Hopmans et al., 2004; Eglinton and Eglinton, 2008
Isotope 13C, 14C of biological marker compound Source of organic materials Ingalls et al. (2006)
PLFA,IPL-Archaea Biomass estimation of bacteria or Archaea White et al., 1979; Lipp et al., 2008 
Crenarchaeol Ammonia-oxidation Archaea Sinninghe Damste et al., 2002
Archaeol Methanogens De Rosa et al., 1986
Plasmalogen Anaerobic bacteria  Villanueva et al., 2007
Cyclopropyl Fatty Acids, trans/cis ratio Environmental stress (Sub-optimal growth or toxic compound) Guckert et al., 1986
UQ/MK Redox state  Villanueva et al., 2007
PHA/PLFA Limited growth factors Villanueva et al., 2007
UK‘37,TEX86 Surface sea temperature Prahl et al., 1988; Schouten et al., 2002

Also important is the quantification of respiration rates - a fundamental life process for microbial biogeochemical functioning. Respiration provides the energy necessary for many ecological processes in an ecosystem, such as the MCP. In MCP-driven biotransformation of LDOC to RDOC, microbial respiration provides direct energy (i.e., ATP) for cellular enzyme syntheses and catalytic reactions such as transportation, modification, fixation and storage of carbon compounds. Thus, a heterotrophic microorganism’s energy production efficiency, which may depend on its respiration efficiency, could determine its MCP efficiency. Aerobically respiring microorganisms possess higher energy production efficiency than anaerobically respiring microorganisms. Thus, an ecosystem that mainly carries out aerobic respiration may have higher ecological MCP efficiency than an ecosystem that respires anaerobically. This distinction may be important in estuarine and coastal ecosystems, where input of nutrients and organic matter due to anthropogenic activities may stimulate intensified heterotrophic respiration processes. These would rapidly consume dissolved oxygen in seawater and sediments, producing extensive hypoxic, and even anoxic zones, in the water column. The reduction of dissolved oxygen and increased nutrient loads, e.g., from terrestrial nitrate, stimulate anaerobic respiration processes, such as nitrate reduction and denitrification. This may have a strong negative impact on the marine ecosystem and even the climate, like the greenhouse gas production (N2O, CH4) by anaerobic microbial processes. In addition, some nutrients may be consumed by anaerobically respiring heterotrophic microorganisms, instead of being available for use by phytoplankton for carbon fixation. In this situation, the ecological function of the estuarine ecosystem is altered and the ecological efficiency is lowered, as less energy is produced and less carbon is fixed. This may also negatively influence the ecological functionality and efficiency of the MCP due to the lowered energy production efficiency. In this project, we will systematically investigate heterotrophic microbial respiration and its influence on the ecological efficiency of carbon storage and the MCP RDOC production, in contrasting oxic, suboxic and anoxic marine environments. 

Evidence for carbon sequestration by the MCP in ancient and modern oceans and potential MCP approaches for carbon sink.

An alternative way to study the geochemical controls on the MCP RDOC reservoir and their climatic effects is to look at ancient oceans, where the MCP was even stronger and the RDOC reservoir larger than in modern oceans. It has been proposed that a DOC reservoir existed in the mid- to late Neoproterozoic (~0.85 to 0.541Ga) oceans, which was at least 102-103 times larger than the modern RDOC reservoir and 104 years longer in its turnover time (Rothman et al., 2003). Given the absence of predators and the dominance of microbial activity in Neoproterozoic oceans, the development of this unusually large RDOC reservoir is generally attributed to the contribution from the MCP. The question now is why the MCP was able to build up a large RDOC reservoir in the deep ocean from during this particular period, rather than at other times in the Proterozoic? The development of this large RDOC reservoir was accompanied not only by the cooling-warming alteration associated with the Neoproterozoic “Snowball Earth” event (Swanson-Hysell et al., 2010), but also by the eukaryotic radiation, which culminated in the earliest animals on Earth (Fike et al., 2006; McFadden et al., 2008). During the Neoproterozoic, a large RDOC reservoir only occurred during the deglacial and warm periods, which contradicts conventional views. These coincidences and contradictions imply that there must be some mechanical links behind them. This sub-project will be specifically designed to explore such links to clarify the geochemical controls on the MCP and its climatic effects. Understanding the MCP dynamics in ancient times could be of great importance for predicting future trends under global change.

Currently there is no international methodological standard of ocean carbon sink, and the focus is on its observation index, corresponding monitoring methods and technology, and an evaluation system and draft standard. To calculate the ocean carbon sink and RDOC/POC reservoir, building an index system includes inorganic carbon parameters (for example, partial pressure of CO2, dissolved inorganic carbon, pH, alkalinity, dissolved oxygen and calcium), organic carbon parameters (for example, refractory dissolved organic carbon, cDOM, fDOM, particle organic carbon), and a series of biological parameters (for example, primary production, new production, community respiration, bacterial respiration and bacterial production). Also included are riverine export fluxes, physical oceanographic parameters, modeling and remote sensors. These are on our agenda. Protocols will be developed to detect cDOM via fluorescence spectrophotometer, analyze DOM components with electrospray ionization mass spectrometry, and analyze age and fractionation of DOC with isotopes of carbon. Detection of POC flux using Th-234 (thorium), primary production using carbon-14 tracing, and new production using a nitrogen-15 method are also profound methods. For the microbial parameters, respiration rates will be calculated using the dissolved oxygen method. INT (a dye that forms crystals inside cells) will be applied to detect cell respiration, etc. We believe this research will help to lay a theoretical foundation for MCP carbon sink research.

Summary statement

Integrating multiple disciplinary approaches, this project is expected to yield much needed information about the mechanisms of RDOC production and transformation in the ocean. The results will also provide insight into the role of DOC in the current global carbon cycle and climate change, shed light on RDOC dynamics in ancient oceans, as well as provide data and information for potential application of the MCP in carbon sequestration engineering in the coastal waters.


This project is supported by the Ministry of Science and Technology of China (No. 2013CB955700). The lipid work will be supported by the State Key Laboratory of Marine Geology and the Chinese national “Thousand Talents Program” award at Tongji University


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Ocean Biological Pump sensitivities and implications for climate change impacts

Anastasia Romanou

Columbia University and NASA-GISS, New York, USA


The ocean is one of the principal reservoirs of CO2, a greenhouse gas, and therefore plays a crucial role in regulating Earth's climate. Currently, the ocean sequesters about a third of anthropogenic CO2 emissions, mitigating the human impact on climate. At the same time, the deeper ocean represents the largest carbon pool in the Earth System and processes that describe the transfer of carbon from the surface of the ocean to depth are intimately linked to the effectiveness of carbon sequestration.

The ocean biological pump (OBP), which involves several biogeochemical processes, is a major pathway for transfer of carbon from the surface mixed layer into the ocean interior. About 75% of the carbon vertical gradient is due to the carbon pump with only 25% attributed to the solubility pump. However, the relative importance and role of the two pumps is poorly constrained (Gruber and Sarmiento 2002; Passow and Carlson 2012). OBP is further divided to the organic carbon pump (soft tissue pump) and the carbonate pump, with the former exporting about 10 times more carbon than the latter through processes like remineralization (Sarmiento et al 2004).

Major uncertainties about OBP, and hence in the carbon uptake and sequestration, stem from uncertainties in processes involved in OBP such as particulate organic/inorganic carbon sinking/settling, remineralization, microbial degradation of DOC and uptake/growth rate changes of the ocean biology. The deep ocean is a major sink of atmospheric CO2 in scales of hundreds to thousands of years, but how the export efficiency (i.e. the fraction of total carbon fixation at the surface that is transported at depth) is affected by climate change remains largely undetermined. These processes affect the ocean chemistry (alkalinity, pH, DIC, particulate and dissolved organic carbon) as well as the ecology (biodiversity, functional groups and their interactions) in the ocean. It is important to have a rigorous, quantitative understanding of the uncertainties involved in the observational measurements, the models and the projections of future changes.

Uncertainties in carbon export

The large uncertainty in the estimates of carbon export (Table 2) is partially explained by the different methodologies (experimental, analytical, numerical), the specific sites of measurements/analysis, the interpolation techniques and the numerical approaches that were used in each study. Mainly however, these discrepancies in global carbon export flux underscore the lack of observational constraints and hence the incomplete understanding of deep processes involved in OBP.

Furthermore, carbon export varies significantly over different time scales. On interannual through decadal time scales, export can change by 0.23-30%, whereas for scales longer than that it may only change within 1-5%. Such variability may also be responsible for the discrepancies in carbon export estimates from observational expeditions that take place at different times of the year, in different years and at different locations.

Table 2. Carbon export estimates from different published studies. Although significant progress has been made, there is still large uncertainty in the amount of carbon that is transported away from the euphotic zone. We need to understand the source of the uncertainties and reduce them.

Source Export (PgC/yr)
Eppley and Peterson 1979 3.4-4.7
Martin et al 1987 6
Falkowski et al 1998 16
Laws et al 2000 11-20
Schlitzer 2002 10
Denman 2003 25
Sabine et al 2004 8
Dunne et al 2005/2007 8-11
Lutz et al 2007 5.7
Henson 2011/2012 5

Because of the large uncertainty range of observational estimates of carbon export, modeling OBP can lead to precarious conclusions. Models use a wide range of parameterizations to describe the fundamental processes involved in OBP, the sensitivity of which, in the parameter space, should be known for each model and always appraised against the observational uncertainties.

Several studies have highlighted the large regional variability of the carbon export (Laws et al 2000; Lutz et al 2007; Henson et al 2011). The largest rates were observed in the upwelling region off Peru, the Ross Sea, the North Atlantic bloom region and the Subtropical Convergence Zones (35o S-45o S) in the Southern Ocean where mode waters form.


Lowest estimates were obtained off Bermuda in the North Atlantic subtropical gyre, at HOT (the site of Hawaii Ocean Time-Series), and in the Eastern Equatorial Pacific during El Niño when upwelling of deep nutrients and primary production in the euphotic layer are reduced. Very low export estimates are given for the Arctic Ocean. Beyond the qualitative agreement though, these studies often disagree quantitatively.

Physics vs. biogeochemistry

The sensitivity of OBP to parameterizations of the recycling of particulate organic carbon in the unforced climate (preindustrial conditions) has been explored in Romanou et al (2013a; 2013b) and was presented at IMBIZO III. Twin control climate simulations were performed using two ocean models coupled to the same atmosphere, land and ice models. The two ocean models (the Russell ocean model and the Hybrid Coordinate Ocean Model, HYCOM) use different vertical coordinate systems, and therefore represent two distinct classes of ocean physics formulation. The Russell model uses a z-like coordinate system, whereas HYCOM uses a hybrid coordinate system in which the vertical grid follows the isobaths in the upper ocean and the isopycnals at depth. Both variants of the GISS climate model were then coupled to the NASA Ocean Biogeochemical Model (NOBM; Gregg and Casey 2007) shown in Fig. 4, which is a functional type based model of chlorophyll and the carbon cycle in the ocean. 


Figure 4. Schematic diagram of the NASA Ocean Biogeochemical Model (NOBM). NOBM includes four functional phytoplankton groups, one heterotrophic group, four nutrients, three detrital pools, DIC and DOC.

Model results showed that the air-sea CO2 flux, the primary production as well as the carbon export are sensitive to ocean model differences due to the different formulations of physical processes such as ventilation, mixing, eddy stirring and vertical advection. However, it was also found that biogeochemical parameterizations such as the treatment of the remineralization affect the model OBP as much as those physical parameterizations. Furthermore, OBP is found to be more sensitive to biological parameterizations in the subtropical front regions of both hemisphere oceans, whereas the oligotrophic subtropical gyres are more sensitive to changes that affect stratification. The Southern Ocean subtropical zone emerged as a key region where the sensitivity to remineralization was robust (of the same order of magnitude in both models).


Uncertainties in OBP reveal the lack of observational evidence to constrain the many processes involved in it, although significant progress has been made in the last decade. Particular attention must be given to estimates of carbon export and variability at shorter as well as longer time scales. At the same time, in models, the large uncertainty reveals a lack of knowledge on how to best parameterize OBP-related processes. Progress along these lines will improve our understanding of how OBP has changed due to anthropogenic perturbations of the global carbon cycle and how it will change in the future due to the changing climate. Given that that many of the OBP uncertainties stem from similar magnitude uncertainties in the biological production in the upper ocean, progress in constraining and parameterizing both OBP and PP needs to be made in parallel.


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Ocean iron fertilization experiments: The dawn of a new era in applied ocean sciences?

Victor Shahed Smetacek

Alfred Wegener Institute, Helmholtz Center for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany 

CSIR National Institute of Oceanography, Goa, India


Ocean iron fertilization (OIF) experiments represent a powerful tool to test ecological hypotheses under natural conditions in the open ocean. They are the marine equivalent of whole-lake experiments in limnology, the results of which have changed our understanding of aquatic ecosystem functioning and lake management techniques in fundamental ways. Decades of close observations of lake ecosystems could not reveal the impact of top predators, via trophic cascades, that came to light in perturbation experiments of entire lakes. Analogously, insights into the impacts of higher trophic levels on the marine pelagial cannot be expected from observational oceanography but need to be obtained from perturbation experiments carried out under natural conditions which includes not only the physics and chemistry of the environment but also the full complement of pathogens, parasites and predators. OIF experiments, if carried out at appropriate scales, offer such an opportunity. In this essay I argue that in situ OIF experiments provide the ideal tool to carry the field forward.  

Unfortunately, OIF has negative connotations in the public but also scientific arenas, because it is associated with geo-engineering schemes to manipulate the climate of our planet. Its application would, it is widely believed, lessen the need to reduce CO2 emissions at the price of eutrophication of the Southern Ocean. Interest in OIF rose after the first two experiments IRONEX I and II, carried out in the HNLC Equatorial Pacific in the mid-1990s, confirmed the first condition of the Iron Hypothesis postulated by the visionary marine biogeochemist John Martin in 1990. The experiments stimulated plankton blooms in the middle of impoverished waters, demonstrating that phytoplankton growth in the open ocean, hence uptake of atmospheric CO2 by the ocean, is limited by the iron supply. They also demonstrated the feasibility of carrying out in situ perturbation experiments in the ocean. Shortly thereafter some venture capitalist companies announced plans to carry out commercial-scale iron fertilization in international waters to claim carbon credits and started patenting possible techniques.

The scientific community reacted to the threat of commercialised geo-engineering by publishing worst-case scenarios of the potential negative effects of large-scale ocean fertilization. Thus, it was postulated that sinking blooms could render subsurface layers anoxic, leading to production of the powerful green-house gases methane and nitrous oxide. Blooms of toxic algae stimulated by OIF were also invoked. The warnings were picked up and magnified by the media and various NGOs that discouraged scientists and their funding agencies from bringing OIF experiments into mainstream research. However, much has changed since then: the internationally binding London Convention has prohibited large-scale ocean iron fertilization (OIF) but expressly allowed scientific experiments, so it is high time for the scientific community to review the potential of iron fertilization experiments in new light.

Iron is a key element controlling productivity of ocean ecosystems and is supplied by dust transported by the atmosphere in a manner akin to rainfall on land. However, unlike water on land, which cannot be recycled within the ecosystem but has to be expelled into the atmosphere by plant transpiration, iron can be stored and recycled by living organisms, in particular the grazers of algae. Indeed, animal biomass on land is only a minute fraction of that of the plants, but in the ocean, heterotrophic biomass on a square meter basis and including the benthos, is always higher. It follows that there is more iron present in heterotrophs, in particular animals, than in photoautotrophs and, because ferric hydroxide (rust) is highly insoluble in sea water, generally much more than in the dissolved inorganic phase.

A good example is the enormous animal biomass contained in the krill stock that was concentrated in the southwest Atlantic Sector of the Southern Ocean up to the first half of the last century. On an areal basis, about twice the amount of iron present in an average diatom bloom was in the krill stock. Prior to their decimation, the great whales are estimated to have consumed at least 150 million tonnes of krill annually, of which the bulk was eaten on the former whaling grounds in the southwest Atlantic Sector. The krill harvest by whales was about double the annual catch of world fisheries over the past decades. Whereas fisheries have resulted in the ocean-wide depletion of fish stocks, krill harvesting by the whales was evidently sustainable, despite its intensity and concentration in a small corner of the ocean. The krill stocks were expected to increase after whale decimation, but observations indicate the opposite has happened: Not only have krill stocks declined over the decades, but primary productivity of the region appears to have declined as well. It is now well established that productivity in the nutrient-rich waters of the Southern Ocean is controlled by the iron supply. The logical explanation for the krill decline, supported by measurements and calculations, is that recycling of iron by whale stocks of the past maintained higher levels of productivity and hence also of krill stocks. The krill biomass acted as a gigantic reservoir of iron that was recycled by whale faeces expelled at the surface in liquid form (Smetacek 2008).


This hypothesis can be tested with iron fertilization experiments carried out along the seasonally retreating sea-ice edge of the former whaling grounds. On the basis of experiments carried out so far, it can be expected that adding iron will lead to development of diatom blooms that will stimulate egg production in adult krill and faster growth rates in juveniles. The iron fertilisation experiments advocated here will need to be specifically designed to mimic the effect of aggregations of feeding whales reported in the past. If deemed successful, larger scale fertilization could be implemented to facilitate krill and whale recovery and would be the equivalent of ecosystem restoration on the high seas.

OIF experiments also open avenues for research on the ecology and behaviour of planktonic protists and their interaction with metazoan grazers. Indeed, the relationship between form and function in the protistan realm is still terra incognita (Smetacek 2012). We marvel at the multitude of intricate shapes in the plankton but do not know their significance. Given that plankton provides the food supply of 70% of the planetary surface and plays a key role in the global carbon cycle, the importance of acquiring this knowledge cannot be over-emphasized. Inroads into this darkness could be made by following changes in community structure over time in a fertilised patch of ocean with the light offered by “-omics” revolution currently underway. Coupled with new techniques for direct observation of plankton in the wild – underwater microscopes – the information could well revolutionise the way we think about how pelagic ecosystems evolved to function the way they do.

The second condition of Martin’s Iron Hypothesis, that biomass from the blooms can sink to great depths so that carbon is sequestered from the atmosphere for long time scales, was confirmed by the EIFEX experiment specifically designed to test it (Smetacek et al. 2012).  The EIFEX site was located in an eddy with high silicate concentrations and large, thick-walled or spiny diatoms dominated the biomass of the bloom because they were less grazed than other phytoplankton groups. Some species from this assemblage underwent mass death, formed sticky aggregates which rapidly sank through the deep water column and presumably formed a layer of fluff on the sea floor. The amount of carbon exported by the flux event (10 g C m-2) was about equivalent to the biomass of an average spring or upwelling bloom. The fate of the other species could not be ascertained as the ship had to leave the site but it is very likely that they too sank into the deep ocean. In the subsequent experiment LOHAFEX, carried out in water with limiting silicate concentrations, the bloom comprised mixed small flagellates that did not contribute to increasing carbon export as did the EIFEX diatoms (Mazzochi et al. 2009).

The results are not really surprising as they confirm field observations: diatoms amongst phytoplankton, are the major contributors to deep carbon export. But this is in contradiction to the widely held view that diatoms are “the pastures of the ocean”. The paradox can be resolved if one differentiates diatoms into groups according to their defences against grazing. This hypothesis, with considerable bearing on the carbon cycle and hence on the future of OIF as a feasible geo-engineering measure, can only be tested in further in situ experiments. Similarly, the hypotheses pertaining to the negative side effects of OIF mentioned in the introductory paragraph can only be tested with more experiments (Smetacek and Naqvi 2008), which, as outlined above, will at the same time provide unparalleled insights into the relationship between ecology and biogeochemistry. Application of large-scale OIF in the Southern Ocean could, at maximum, enhance the natural annual export by about 10%, i.e. 1 Gt. Compared to the current rate of atmospheric accumulation of about 4 Gt, this is not much. However, there is no other technique available that can remove as much over long time scales: it is too little to be a solution, but too much to ignore. It certainly justifies further exploration. If ever applied on a large-scale, OIF should be carried out by a non-profit international agency analogous to various UN organisations such as the IAEA, WHO or FAO. See Smetacek (2013) for more details.



  • Martin, J. H., 1990. Glacial-interglacial CO2 change: The iron hypothesis. Paleoceanography 5: 1-13.
  • Mazzochi, M.G., González, H.E., Vandromme, P., Borrione, I., Ribera d’Alcalà, Gauns, M., Assmy, P., Fuchs, B., Klaas, C., Martin, P., Montresor, M. Ramaiah, N., Naqvi, S.W., Smetacek, V., 2009. A non-diatom plankton bloom controlled by copepod grazing and amphipod predation: Preliminary results from the LOHAFEX iron-fertilization experiment. GLOBEC International Newsletter, October 2009, 1-4.
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  • Smetacek, V. and Naqvi, S.W.A., 2008. The next generation of iron fertilization experiments in the Southern Ocean. Phil Trans. R. Soc. A 366: 3947-3967. 
  • Smetacek, V., Klaas, C., Strass, V.H., Assmy, P., Montresor, M., Cisewski, B., Savoye, N. Webb, A, d’Ovidio, F., Arrieta, J.M., Bathmann, U., Bellerby, R., Berg, G.M., Croot, P., Gonzalez, S., Henjes, J., Herndl, G.J., Hoffmann, L.J., Leach, H., Losch, M., Mills, M.M., Neill, C., Peeken, I., Röttgers, R., Sachs, O., Sauter, E., Schmidt, M.M., Schwarz, J., Terbrüggen, A., Wolf-Gladrow, D., 2012. Deep carbon export from an iron-fertilized Southern Ocean diatom bloom. Nature 487, 313-319. doi:10.1038/nature11229. (See also comments posted on the Nature website).
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Human-Ocean-Human Interactions

Social-ecological change, thresholds and governance in aquatic-terrestrial systems (A research project supported by the Canada SSHRC-Banting (Social Sciences and Humanities Research Council) Fellowship Program

Prateep Kumar Nayak

Environmental Change and Governance Group (ECGG), Faculty of Environment, University of Waterloo, Canada



A key challenge for governance is to understand the emergence of thresholds and the potential for regime shifts in social-ecological systems (Folke 2006). Thresholds of change can be seen as a breakpoint between two alternative system configurations (Walker and Myers 2004). Regime shifts are sudden, often irreversible and large-scale changes in the system, whereby a threshold is passed and the core functions, structure, and processes of the new regime are fundamentally different from the previous regime (Scheffer and Carpenter 2003). Identification of ecological drivers of thresholds and regime shifts has improved with numerous examples in aquatic and terrestrial systems (Biggs et al. 2009; Scheffer 2009). Despite such advances, understanding of linked social-ecological variables that may possibly signal approaching thresholds and regime shifts and the implications for governance remains poor (Walker and Meyers 2004; Scheffer and Carpenter 2003; Béné et al. 2011). In this context, governance approaches must identify, acknowledge and navigate impending thresholds before they are crossed, or address the often undesirable consequences of regime shifts when they do occur. Three objectives guide this research to examine some of these aspects:

1) To draw on socially and ecologically defined thresholds and understanding of key variables to define appropriate social-ecological units for governance.

2) To identify and assess emerging governance arrangements for multi-resource sector social-ecological units experiencing rapid change.

3) To compare and synthesize experience with adaptive, multi-level governance processes across study sites and identify their potential for dealing with uncertainty.

Relevant scholarly literature  

The need to understand governance and sustainability in the context of social-ecological systems is well established (Hollings 2001; Berkes et al. 2003; Folke et al. 2005; Lebel et al. 2006). Strategies to do so are less clearly articulated. A social-ecological system perspective reflects the integration of humans in nature whereby human actions affect biophysical systems, biophysical factors affect human well-being, and humans in turn respond to these factors (Berkes and Folke 1998; Berkes 2011). Thus, both social and ecological processes define and shape the nature of governance arrangements (Folke et al. 2005). Using this perspective, social-ecological units of governance can be seen as integrated, coupled, interdependent and co-evolutionary human-environment systems (Turner et al. 2003; Berkes 2011) that stress key relationships (MEA 2005), interactions (Kates et al. 2001) and connections (Nayak 2011; Nayak and Berkes 2012) between people and their environment. Defining appropriate social-ecological units of governance requires an understanding of how multi-scale drivers of change and interactions among key system variables may cross critical thresholds and lead to regime shifts.

Thresholds and regime shifts are critical but they are very difficult to detect. A resilience perspective helps to understand the capacity of a system to absorb disturbance and reorganize while undergoing change so as to still retain essentially the same function, structure, identity, and feedbacks (Walker et al. 2004) and possibly help the system to steer through threshold changes and regime shifts. Identifying variables and key indicators to understand the dynamics involved in threshold changes is important, especially from a governance perspective. While ecological thresholds in relation to the use of ecosystems is better recognised (Walker and Myers 2004; Resilience Alliance and Santa Fe Institute 2011), socially and culturally relevant thresholds and indicators will provide an alternate way of conceiving change in complex systems (Béné et al. 2011).

Different perspectives on governance also offer insights on thresholds, regime shifts and change. Governance is defined here as “the interrelated and increasingly integrated system of formal and informal rules [institutions], rule-making systems, and actor-networks at all levels of human society (from local to global) that are set up to steer societies towards preventing, mitigating, and adapting to global and local environmental change” (Biermann et al. 2009). Of particular relevance here is the notion of adaptive governance, which expands the focus from adaptive management of ecosystems to address the broader social contexts that enable ecosystem-based management (Dietz et al. 2003; Folke et al. 2005; Carpenter and Folke 2006). Institutions are crucial for governance as they have the ability for renewal and reorganisation, learning and adaptation, interactions and linkages and in dealing with change in both the social and biophysical systems (Holling 2001; Berkes et al. 2003; Ostrom 2005).


Four insights result from the preceding discussion. First, while integration of social and ecological aspects is recognized as a crucial element of governance, how this understanding can be extended to identify appropriate social-ecological units, across aquatic-terrestrial resource systems, is poorly understood. Developing key indicators and criteria to define the boundaries of social-ecological units of governance is a priority.

Second, thresholds of change are important indicators of undesirable regime shifts. An understanding of thresholds and regime shifts can provide a lens with which to frame key governance questions and the scope for institutional innovations. A focus on generating socially and ecologically defined thresholds and their variables will address this gap.

Third, “institutional interplay” (Young 2002; Grilo 2011) and the “fit” between the institutions and the dynamics of biophysical systems (Folke et al. 2007; Young 2006) represent a significant governance challenge. Mismatch between ecological and social dynamics and deviation of institutional boundaries from resource or ecosystem boundaries (Folke et al. 2007; Berkes 2006) is a particular challenge given the speed and intensity of social-ecological change.

Fourth, there is a need for policy and practice to reinforce core attributes of governance systems and facilitate patterns of development that promote human well-being while conserving the life support systems of the planet (MEA 2005; Levin and Clark 2010).


Significance and anticipated contribution to knowledge and practice 

The research aims to generate novel insights on governance of social-ecological systems experiencing rapid change. The implication of thresholds for governance of social-ecological systems (SES) is emphasized. Case-based participatory strategies in the Chilika Lagoon, India and the Tam Giang Lagoon, Vietnam and meta-analysis are employed to understand thresholds and the implications for governance from the standpoint of resource users as well as from natural science perspectives (Béné et al. 2011). The program of research will make significant contributions to knowledge and practice in many specific ways:

1. It enhances our understanding of SES thresholds and possible regime shifts. This is especially relevant since attempts to analyze thresholds have been hampered by a lack of readily available empirical data (Walker and Meyers 2004).

2. Extending the focus on socially and culturally relevant thresholds, in addition to ecologically defined thresholds, is an innovation in this research. An important outcome will be a novel, participatory and integrative way to understand thresholds and key variables (Béné et al. 2011) in linked aquatic-terrestrial systems.

3. It extends our understanding of integrated SES by helping to define appropriate units of governance involving aquatic-terrestrial resources. An applied understanding in this regard is critical, as is the development of integrative theory to better characterize, explain, and predict governance models that can steer such SESs to sustainability either by avoiding critical thresholds or purposefully crossing them to navigate away from undesirable states (Armitage and Plummer 2010).

4. This research will generate evidence-based lessons and best practices for governance of linked aquatic-terrestrial systems, while also extending the literature on environmental governance, particularly its contributions to sustainability of multi-resource sector SESs.

5. While concepts and frameworks are essential, the research will take this work further by creating an opportunity to link theory to practice and public policy. A related focus will be on developing implementation and assessment tools for use by practitioners, managers and policy makers - an effort consistent with recent initiatives on developing diagnostic tools for governance and sustainability (Ostrom 2007; Pahl-Wostl 2009: Evans and Andrew 2011; Béné et al. 2011).


For more details on the project please contact Dr Prateep Kumar Nayak at pnayak@uwaterloo.ca


  • Armitage, D. and Plummer, R. (Eds.), 2010. Adaptive Capacity and Environmental Governance. Berlin: Springer.
  • Béné, C., Evans, L., Mills, D. et al., 2011. Testing resilience thinking in a poverty context: Experience from the Niger River basin. Global Environmental Change 21: 1173 – 1184.
  • Berkes. F., 2006. From community-based resource management to complex systems: The scale issue and marine common. Ecology and Society 11(1): 45. [Online] URL: http://www.ecologyandsociety.org/vol11/iss1/art45/
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  • Berkes, F. and Folke, C. (eds), 1998. Linking Social and Ecological Systems: Management Practices and Social Mechanisms for Building Resilience. Cambridge: Cambridge University Press.
  • Berkes, F., Colding, J., and Folke, C. (eds), 2003. Navigating Social-Ecological Systems: Building Resilience for Complexity and Change. Cambridge: Cambridge University Press.
  • Biermann, F., Betsill, M. M., Gupta, J., Kanie, N., Lebel, L., Liverman, D., Schroeder, H., Siebenhüner, B., Conca, K., da Costa Ferreira, L., Desai, B., Tay, S., and Zondervan, R., 2009. Earth System Governance: People, Places and the Planet. Science and Implementation Plan of the Earth System Governance Project, ESG Report No. 1. Bonn, IHDP: The Earth System Governance Project.
  • Biggs, R., S. R. Carpenter and W. A. Brock., 2009. Turning back from the brink: Detecting an impending regime shift in time to avert it. Proceedings of the National Academy of Science 106 (3): 826 – 831.
  • Carpenter, S. R., 2003. Regime shifts in lake ecosystems: pattern and variation. In: Kinne, O. (ed). Excellence in Ecology: 15. Germany: International Ecology Institute.
  • Dietz, T., Ostrom, E., and Stern, P., 2003. The struggle to govern the commons. Science 302: 1907-1912.
  • Evans, L and Andrew, N. L., 2011. Diagnosis and the management constituency of small-scale fisheries. In: N. Andrew and R. Pomeroy, (eds). Small-scale Fisheries Management Frameworks and Approaches for the Developing World. Wallingford: CABI Publishing.
  • Folke, C., 2006. Resilience: The emergence of a perspective for social–ecological systems analyses. Global Environmental Change 16: 253-267.
  • Folke, C., Hahn, T., Olsson, P., and Norberg, J., 2005. Adaptive governance of social-ecological systems. Annual Review of Environment and Resources. 30: 441-473.
  • Folke, C., Pritchard, L., Berkes, F., Colding, J., and Svedin, U., 2007. The problem of fit between ecosystems and institutions: Ten years later. Ecology and Society 12(1): 30. [Online] URL: http://www.ecologyandsociety.org/vol12/iss1/art30/
  • Grilo, C., 2011. Institutional interplay in networks of marine protected areas with community-based management. Coastal Management 39(4): 440-458.
  • Holling, C. S., 2001. Understanding the complexity of economic, ecological, and social systems. Ecosystems 4: 390-405.
  • Kates, R., Clark, W. C., Corell, R., et al., 2001. Sustainability science. Science 292: 641-642.
  • Lebel, L., Anderies, J. M., Campbell, B., Folke, C., Hatfield-Dodds, S., Hughes, T. P., and Wilson, J., 2006. Governance and the capacity to manage resilience in regional social-ecological systems. Ecology and Society 11(1): 19. [Online] URL: http://www.ecologyandsociety.org/vol11/iss1/art19/
  • Levin, S. A., and Clark, W. C. (eds), 2010. Toward a Science of Sustainability: Report from Toward a Science of Sustainability Conference, Airlie Center, Warrenton, Virginia, November 29, 2009 – December 2, 2009. CID Working Paper No. 196. Center for International Development at Harvard University.
  • MEA (Millennium Ecosystem Assessment). 2005. Ecosystems and human well-being: General synthesis. In: Millennium Ecosystem Assessment. Chicago, IL, USA: Island Press. [Online] URL: http://www.Millenniumassessment.org/en/Synthesis.aspx
  • Nayak, P. K., 2011. Conditions for Governance of tenure in lagoon social-ecological systems: Lessons from around the world. UN/FAO initiative on Governance of Tenure for Responsible Capture Fisheries. Rome: FAO.
  • Nayak. P. K. and Berkes, F., 2012. Linking global drivers with local and regional change: A social-ecological system approach in Chilika Lagoon, Bay of Bengal. Regional Environmental Change Online First, DOI 10.1007/s10113-012-0369-3
  • Ostrom, E., 2005. Understanding Institutional Diversities. Princeton, USA: Princeton University Press.
  • Ostrom, E., 2007. A diagnostic approach for going beyond panaceas. Proceedings of the National Academy of Science 104 (39): 15181-15187.
  • Pahl-Wostl, C., 2009. A conceptual framework for analysing adaptive capacity and multi-level learning processes in resource governance regimes. Global Environmental Change 19(3): 354-365.
  • Resilience Alliance and Santa Fe Institute. 2004. Thresholds and alternate states in ecological and social-ecological systems. Resilience Alliance. [Online] URL: http://www.resalliance.org/index.php?id=183
  • Scheffer, M., 2009. Critical Transitions in Nature and Society. Princeton, USA: Princeton University Press
  • Scheffer, M. and Carpenter, S. R., 2003. Catastrophic regime shifts in ecosystems: linking theory to observation. Trends in Ecology and Evolution 18(12): 648–656.
  • Walker, B. and Meyers, J. A., 2004. Thresholds in ecological and social–ecological systems: a developing database. Ecology and Society 9(2): 3. [Online] URL: http://www.ecologyandsociety.org/vol9/iss2/art3/
  • Walker, B., Holling, C. S., Carpenter, S. R., and Kinzig, A., 2004. Resilience, adaptability and transformability in social-ecological systems. Ecology and society 9(2):5. [Online] URL: http://www.ecologyandsociety.org/vol9/iss2/art5
  • Young, O., 2002. The Institutional Dimensions of Environmental Change: Fit, Interplay and Scale. Cambridge: MIT Press.
  • Young, O., 2006. Vertical interplay among scale-dependent environmental and resource regimes. Ecology and Society 11(1): 27. [Online] URL: http://www.ecologyandsociety.org/vol11/iss1/art27/
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Reduced pressure in the Israeli coastal ecosystem: Remediation by means of policy change

Dror Angel1,2,*, Dor Edelist2, Shirra Freeman2,3, Noa Nakar1

1 Department of Maritime Civilizations, Charney School for Marine Science, University of Haifa, Mt Carmel, Haifa 31905, Israel

2 Leon Recanati Institute for Maritime Studies, University of Haifa, Mt Carmel, Haifa 31905, Israel

3 Braun School of Public Health and Community Medicine, Hebrew University of Jerusalem, Hadassah Ein Kerem, Jerusalem 91120, Israel

* adror@research.haifa.ac.il

The eastern Mediterranean Sea has been noted as one of the world’s most oligotrophic regions, boasting record Secchi disk depths, extending almost 60m below the surface and extremely low levels of nutrients and chlorophyll (Azov 1991). Despite fairly low levels of primary production, the region supports a moderate fishery with annual Israeli landings exceeding 4000t, equally distributed over trawling, purse-seining and inshore fisheries. During the 1970s, the pelagic fishery began declining. In part, this was because of lower yields hypothesized to be the result of disruption caused by the damming of the Nile. The primary reason was the increasing availability of cheaper imported fish that flooded Israeli markets and the signing of free commerce pacts between Israel and the European Union. Since the 1980s, coastal gillnet and longline yields have been in steady decline, and the number of inshore artisanal fishers has dropped. Today fishing is the main source of income for one third of Israel’s inshore fishers and most landings in Israel come from bottom trawling. 

A review of the state of the eastern Mediterranean Sea over the past 60 years reveals an increase in mean seawater temperature and salinity, a drop in productivity, diversity and fish landings and a change in the composition of the fish caught. The 2.5 fold drop in fish landings per unit effort over the past 50 years (Fig. 5) is a clear sign of overfishing and has affected the value of landings. Fishery data show that there has been a steady increase in the numbers of non-endemic species (especially in shallow waters; Fig. 6), and a concomitant rise in the by-catch, increased abundance of toxic fish and a decrease in the mean size of fish caught. Specific changes include an increase in the landings of crustaceans, from 23 – 36% over the past 20 years, and a drop in mean trophic level of landings. Some of the faunal changes observed are probably related to climate and regional changes, but other factors are clearly involved, including a decline in the supply of sand from the Nile delta, changes in coastal water quality, overfishing, arrival of exotic organisms via the Suez Canal and by means of vectors, radical changes in intertidal and subtidal habitats as a result of coastal development, etc.


Figure 5. Catch Per Unit Effort (in Kg per Horse Power (HP) per fishing day) of Israeli trawlers from 1950 to 2008. Calculated from the Israel Department of Fishery Statistical Yearbooks. (Derived from Edelist et al. 2011).


Figure 6. Differences between past and present catch on the Levantine shelf. The number of specimens caught per hour of trawling + one standard error for the 25 demersal species which contributed most to dissimilarity between 1990-4 (open bars) and 2008-11 (solid bars). The arrival and rapid proliferation of new invasive species (top) are mirrored by declines of indigenous species (bottom), the rarest of which are at the brink of extirpation and underline the shift in community composition over the last two decades. *P0.002. (Derived from Edelist et al. 2013).


Whereas there is clear evidence of ecological change in the eastern Mediterranean, the area has been largely under-studied and aside from the reported changes in fishery landings, and some of the invertebrate species (Galil 2012), we know very little about the dynamics of other groups in the marine ecosystem. In the late 1970s and early 1980s increasing abundances of Rhopilema nomadica (Fig. 7), a newly arrived scyphomedusa were observed along the Israeli Mediterranean beaches. This stinging jellyfish appeared in annual blooms, generally in the summer months, and in the early years was mainly a nuisance to beach-goers. The medusa blooms were eventually renamed “swarms” as these increased in size, duration and effects. In addition to their impacts on coastal recreation, the medusae affect the functioning of essential coastal installations, such as the electric and desalination utilities by clogging the seawater water intake systems, and local fisheries (Fig. 8). A recent study of jellyfish and Israeli fishers indicates that jellyfish have both direct and indirect impacts on this sector. Direct impacts include damage to nets and gear, loss of fishing days and physical injury to the fishermen, whereas indirect impacts include competition of medusae with finfish over the same food source and predation of jellyfish on juvenile fish and eggs. These indirect impacts on the fisheries implicate jellyfish as another source of disruption of the balanced function of the marine ecosystem.



Figure 7. Invasive scyphomedusan, Rhopilema nomadica (photo: Amir Yurman).


Figure 8. Contents of a trawl net during a bloom of Rhopilema nomadica, Haifa Bay, June 2011 (photo: Dor Edelist).

As the number of stressed endemic fish species grows, it is imperative that we implement management systems that enable stock regeneration (Edelist et al. 2013). Management may be achieved by means of policies or strategies that combine seasonal moratoria, marine protected areas and restrictions on fishing practice. The first aims to restrict catches during particularly sensitive periods, such as spawning. The second aims at providing more comprehensive protection and serves as a limited biosphere or buffer to facilitate undisturbed ecosystem function, especially for particularly sensitive or important ecosystem functions (e.g. spawning grounds, protected areas for juveniles and other key habitats). The third aims mainly at protecting habitat, limiting catch size, the size of fish caught and by-catch. Although these strategies take some time to bear fruit, it is likely, as found in those areas where MPA programs have succeeded, that wild fish stocks will eventually rebound, and that the invasive nuisance species are likely to subside. It is also noteworthy that in order to be effective, such management measures need to be carried out at a regional level, and not only by a single country. 


  • Azov, Y., 1991. Eastern Mediterranean – a marine desert? Marine Pollution Bulletin 23: 225–232.
  • Edelist, D., Rilov, G., Golani, D., Carlton, J.T., Spanier, E. 2013. Restructuring the Sea: profound shifts in the world's most invaded marine ecosystem. Diversity and Distribution 19: 69-77.
  • Edelist, D., Sonin, O., Golani, D., Rilov, G. and Spanier, E. 2011. Spatiotemporal patterns of catch and discards of the Israeli Mediterranean trawl fishery in the early 1990s: ecological and conservation perspectives. Scientia Marina 75(4): 641-652.
  • Galil, B.S., 2012. Truth and consequences: the bioinvasion of the Mediterranean Sea. Integrative Zoology 7: 299–311.
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IMBER-CLIVAR joint initiative on upwelling

Ken Drinkwater

Institute of Marine Research, Bergen, Norway

At the 2012 joint meeting of Scientific Steering Committees of IMBER and CLIVAR, it was proposed to begin joint studies on marine biophysical interactions and the dynamics of upwelling systems. 

Why focus on upwelling systems?  Upwelling regions of the oceans are the most productive fisheries areas in the world. For example, approximately 7% of primary production and 20% of the total global marine fish catches come from eastern boundary upwelling areas alone, but these occupy <2% of the total ocean area (Pauly and Christensen, 1995). These include the Humboldt Current off Peru, the California Current, the Northeast Atlantic off the Iberian Peninsula and NW Africa, and the Benguela Current off southern Africa. These are examples of coastal upwelling driven by wind-induced Ekman divergence against a coastline. Such upwelling also occurs around Antarctica owing to the mean anticyclonic winds. Seasonal upwelling, due to reversal of winds caused by monsoons, are also important in regions such as the Arabian Sea and the Bay of Bengal. Upwelling favourable winds force near surface waters offshore to be replaced by colder, lower oxygenated, high nutrient-rich waters. This often results in high primary production near surface that can be readily observed as high chlorophyll-a regions in satellite imagery (Fig. 9). Anoxia and hypoxia can occur in the near bottom waters around upwelling regions (Chan et al., 2008). 

Other types of upwelling systems exist such as in western boundary currents, e.g. the Kuroshio, the Gulf Stream, the Agulhas Current, and the East Australian Current. These currents, being in approximate geostrophic balance, have a strong tilt in the density surfaces upwards towards the shelf. Velocity changes in the currents lead to variability in the pycnocline depth and can bring cold nutrient-rich water onto the shelf. This is called dynamic uplift. Likewise, an eddy that bumps up against the shelf can also lift the pycnocline up and onto the shelf. Upwelling also occurs along the Equator owing to the trade winds, coupled with the change in the sign of the Coriolis force across the Equator. This upwelling leads to increased phytoplankton production around the Equator that is clearly seen in satellite imagery. 


Figure 9. Chlorophyll-a concentrations off the western coast of Mexico from the MODIS (Aqua) satellite in November 2004. Obtained from: www.jcsda.noaa.gov/documents/meetings/WARSO2007/GrodskyOceanObs08011500.pdf


In spite of their importance, upwelling systems typically are poorly represented in global models owing to their relatively small spatial scales. This results in warm temperature biases in these regions within the models. Merging a regional climate model of the California Current System into a global model, Curchister et al. (2011) were able to show much reduced biases, even stretching into the North Atlantic Ocean. Rykaczewski and Dunne (2010) showed the importance of considering basin-scale physics in understanding regional upwelling dynamics. Even if the ocean models were able to produce the 'correct' amount of upwelling, the characteristics of upwelling water masses can be wrong. This can be a result of problems with the ocean’s interior circulation, the upwelled water masses including their dissolved oxygen and nutrient concentrations, and/or stratification. Remote forcing and large-scale climate indices can also influence the amount of upwelling (Fig. 10) and may explain differences between upwelling regions under similar local forcing (Richter et al., 2010).


Figure 10. The North Pacific Gyre Oscillation (NPGO) forcing pattern (left panel) and the correspondence between the Coastal Current Upwelling Index off California and the NPGO index (right panel) taken from Di Lorenzo et al. (2008).

The rate and duration of upwelling influences the amount of biological production as well as the occurrence of hypoxia. The upwelling rate determines the phytoplankton cell size, with small phytoplankton dominating when the upwelling rate is too high or too low. Nutrient stoichiometry of the upwelled water can also impact cell size, e.g., upwelling in high nutrient, low chlorophyll regions are dominated by small cells due to iron limitation. Small cells result in reduced production of fish since small phytoplankton production is mainly channeled through a microbial food web before reaching fish. This adds extra trophic levels between the algae and the fish, and subsequently a loss of energy. On the other hand, with a moderate rate of upwelling, large size phytoplankton dominate and production can be transferred more directly to fish via large zooplankton grazers (e.g. Van der Lingen et al. 2011). This leads to a more efficient energy transfer and higher fish production. Thus, knowledge of the mechanisms controlling the rate and duration of upwelling is important for understanding the fish production.


Current global and regional biophysical models have focused mainly on the physics and the lower trophic levels, i.e. phytoplankton and zooplankton. Efforts to extend regional models to higher tropic levels, e.g. fish, are making progress but few of these have focused on upwelling regions. While including fish greatly increases the model complexity, such models are progressing and offer great potential for progress in terms of our ecosystem understanding. Greater effort is needed to apply such models in upwelling regions. The wasp-waist ecosystem control model has been assumed to be present in all upwelling ecosystems, and to be different than other systems (Cury et al., 2000). This model states that an intermediate trophic level (such as sardines or anchovies) controls the abundance of predators through a bottom-up interaction and the abundance of prey through a top-down interaction However, this assumption is now being questioned (Madigan et al., 2012). Resolving this issue will be important for developing end-to-end ecosystem models of upwelling regions. Fisheries in eastern boundary upwelling systems (EBUS) are usually dominated by small pelagic schooling fish. Such regions are often characterized by the alternation of anchovy and sardine periods on the multi-decadal scale (Schwartzlose et al. 1999), e.g. in the Humboldt Current.  Switching between these different production regimes has been traced back for the last two millennia based on analysis of California Current sediment samples (Baumgartner et al. 1992). Climate-driven changes in basin-scale circulation seem to control zooplankton dynamics in the California Current (Keister et al. 2011) and there is evidence that the dynamics of sub-tropical and sub-polar gyres affect productivity regimes in other EBUS. Investigations are needed on spatial distribution of the productivity. For example, some of the upwelling-derived production is retained in coastal locations (such as the Southern California Bight or Vizcaino Bay in the California Coastal System, or Talcahuano in Humboldt). Little is known of the physical characteristics that lead to the high production in such areas, although higher retention is expected. The relative amount of production in such embayments compared to that offshore is unclear, as is the energy flow efficiency and total fish production in such areas.

One of the major issues of our day is anthropogenic climate change.  Bakun (1990) proposed that increased winds under climate change will result in increased upwelling, a result supported by temperature data from the California Current system. Evidence for recent increased upwelling has also been found in other upwelling regions (e.g. McGregor et al., 2007; Narayanan et al., 2010) but decreased upwelling has occurred off the Canaries (Gomez-Gesteira et al., 2008) and no trend has been detected off Peru (Demarcq, 2009). Further work on the upwelling trends under climate change is needed to determine the balance between cooling due to increased upwelling (where it exists) and warming due to climate change. 

To consider possible major research questions that an upwelling research initiative should address, a working team was assembled consisting of scientists from both IMBER and CLIVAR, as well as representatives from the IOC and the former GLOBEC regional program on small pelagics (SPACC).  As of early 2013, the team considered the following as possible topics of joint inquiry:

  • What controls interannual variability in upwelling systems?
  • What is the interaction between upwelling and large-scale atmospheric climate systems?
  • What is the role of upwelling systems in shaping mean biases in coupled climate models reducing predictability in those regions?
  • What is the connection between large-scale climate indices (ENSO, PDO, NAO, AMO/AMV, etc.) and upwelling?
  • How do physical upwelling dynamics affect ecological responses?
  • What is the role of upwelling on the oxygen levels in such zones? 
  • How does upwelling affect biogeochemical processes and the microbial loop?
  • How does the combination of climate and fisheries affect the ecological dynamics of upwelling ecosystems, including exploited species such as small pelagic fish? Can a better understanding be achieved to inform management and policy?
  • What is the expected physical response in the upwelling areas under climate change?
  • How will these changes affect plankton and fisheries production?

These were reported to the 2013 Scientific Steering Committee meetings of IMBER and CLIVAR for discussion. As a result, the team has been asked to develop an implementation plan to tackle 2-3 issues of joint interest through workshops and/or working groups. One research effort has already begun on upwelling in the Eastern Indian Ocean through the joint efforts of IMBER’s SIBER (Sustained Indian Ocean Biogeochemistry and Ecosystem Research) regional programme and CLIVAR’s Indian Ocean Panel. Their first international workshop took place in April 2013 in Japan, and the second will take place in November in China to develop the Science Plan and Implementation Strategy. There will be a third workshop during the IMBER Open Science Conference in Bergen, Norway in June 2014.

Future plans and activities of the IMBER/CLIVAR upwelling research initiative will be broadcast as they develop.  Stay tuned! 


  • Bakun, A., 1990. Global climate change and intensification of coastal ocean upwelling. Science 247: 198-201.
  • Baumgartner, T. R., Soutar, A., Ferreira-Bartrina, V., 1992. Reconstruction of the history of Pacific sardine and northern anchovy populations over the last two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep. 33: 24–40.
  • Chan, F., Barth, J. A., Lubchenko, J., Kirinich, A., Weeks, H., Peterson, W. T., Menge, B. A., 2008. Emergence of anoxia in the California Current Large Marine Ecosystem, Science, 319: 920.
  • Curchitser, E., Small, J., Hedstrom, K., Large, W., 2011. Up- and down-scaling effects of upwelling in the California Current System. pp. 98-102. In: Foreman, M.G., Yamanaka, Y. (Eds), Report of Working Group 20 on Evaluations of Climate Change Projections, PICES Scientific Report No. 40.
  • Cury, P., Bakun, A., Crawford, R.J.M., Jarre, A., Quinones, R.A., Shannon, L.J., Verheye, H.M., 2000. Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES Journal of Marine Science 57: 603-618.
  • Demarcq, H., 2009. Trends in primary production, sea surface temperature and wind in upwelling systems (1998-2007). Progress in Oceanography 83: 376-385.
  • Di Lorenzo, E., Schneider, N., Cobb, K.M., Franks, P.J.S., Chhak, K., Miller, A.J., McWilliams, J.C., Bograd, S.J., Arango, H., Curchitser, E., Powell, T.M., Rivière, P., 2008. North Pacific Oscillation links ocean climate and ecosystem change. Geophysical Research Letters 35, L08607, doi:10.1029/2007GL032838.
  • Gomez-Gesteira, M., De Castro, M., Alvarez, I., Lorenzo, M.N., Gesteira, J.L.G., Crespo, A.J.C., 2008. Spatio-temporal upwelling trends along the Canary upwelling system (1967-2006). Annals of the New York Academy of Sciences 1146: 320-337.
  • Keister, J.E., Di Lorenzo, E., Morgan, C.A., Combes, V., Peterson, W.T., 2011. Copepod species composition linked to ocean transport in the Northern California Current. Global Change Biology 17: 2498–2511.
  • Large, W.G., Danabasoglu, G., 2006. Attribution and impacts of upper-ocean biases in CCSM3. Journal of Climate 19: 2325–2346.
  • Madigan, D.J., Carlisle, A.B., Dewar, H., Snodgrass, O.E., Litvin, S.Y., Micheli, F., Block, B.A., 2012. Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem. Scientific Reports 2, 654. doi:10.1038/srep00654.
  • McGregor, H.V., Dima, M., Fischer, H.W., Mulitza, S., 2007. Rapid 20-th Century increase in coastal upwelling off Northwest Africa. Science 315: 637-639.
  • Narayan, N., Paul, A., Mulitza, S., Schulz, M., 2010. Trends in coastal upwelling intensity during the late 20th century. Ocean Science Discussions 7, 335-360.
  • Pauly, D., Christensen, V., 1995. Primary production required to sustain global fisheries. Nature 374: 255-257.
  • Richter, I., Behera, S.K., Masumoto, Y.,Taguchi, B., Komori, N., and Yamagata, T., 2010. On the triggering of Benguela Niños: Remote equatorial versus local influences, Geophysical Research Letters 37, L20604. doi:10.1029/2010GL044461.
  • Rykaczewski, R.R., Dunne, J.P., 2010. Enhanced nutrient supply to the California Current Ecosystem with global warming and increased stratification in an earth system mode. Geophysical Research Letters 37, L21606, doi:10.1029/2010GL045019.
  • Schwartzlose R., Alheit, J., Bakun, A., Baumgartner, T., Cloete, R., Crawford, R., Fletcher, W., Green-Ruiz, Y., Hagen, E., Kawasaki, T., Lluch-Belda, D., Lluch-Cota, S., Maccall, A., Matsuura, Y., Nevárez, M., Parrish, R., Roy, C., Serra, R., Shust, K., Ward, M., Zuzunaga, J., 1999. Worldwide Large-scale fluctuations of sardine and anchovy populations. South African Journal of Marine Science 21: 289-347.
  • van der Lingen, C.D., Bertrand, A., Bode, A., Brodeur, R., Cubillos, L., Espinoza, P., Friedland, K., Garrido, S., Irigoien, X., Möllman, C., Rodriguez-Sanchez, R., Tanaka, H., Temming, A., 2009. Chapter 7. Trophic dynamics. In: Checkley, D.M., Roy, C., Alheit, J.,Oozeki, Y. (Editors), Climate change and small pelagic fish. GLOBEC Project Office, Plymouth (UK), pp. 112-157.
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New to IMBER!

New endorsed projects

Sustainability of Marine Ecosystem Production under multi-stressors and Adaptive Management (MEcoPAM)

The sustainability of marine ecosystem production is impacted by multi-stressors, such as physical processes, eutrophication, over-fishing and aquaculture. The objectives of the MEcoPAM project are to identify and characterize the interactions of marine biogeochemical cycles and marine ecosystems, and to understand the response of typical marine ecosystem production to multi-stressors, thereby improving our knowledge of the impact of multi-stressors on the sustainability of marine ecosystem production.

The research areas include several unique sub-ecosystems in the Bohai Sea, Yellow Sea, and East China Sea (e.g. the hypoxia zone off the Changjiang Estuary, and aquaculture sites in the Shandong Peninsula). The major scientific questions to be addressed are:

  • What is the impact of multi-stressors on biogeochemical cycles in coastal ecosystems (e.g. hydrodynamic control of biogenic element cycles, coupling mechanism of primary production with biogeochemical processes)?
  • How does ecosystem functioning in the hypoxia zone of the East China Sea respond to multi-stressors (e.g. the role of metabolism and redox processes on element cycles, impact of hypoxia on the function and structure of marine ecosystem, impact of open ocean and atmosphere)?
  • What adaptive strategies of coastal aquaculture ecosystems to deal with multi-stressors (e.g.  the supporting role of main biogeochemical processes in food production and food web trophodynamics of major biological functional groups, adaptive strategies to fishery management)?

In addition to field observations of the physical, chemical and biological properties of ecosystems in East China Sea, Changjiang Estuary and the coastal area of the Shandong Peninsula, historical data analysis, numerical modelling and microcosm experiments will be undertaken.

More info...

MEcoPAM website (Chinese)
MEcoPAM website (English)

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Variability of Ocean Ecosystems around South America (VOCES)

The overall goal of this project is to assess the impact of climate variability - both natural and anthropogenic - on the Humboldt, Patagonia and South Brazil Large Marine Ecosystems. These ecosystems are amongst the most productive of the southern hemisphere, sustaining more than 20% of the global fish catch, hosting unique biodiversity and with CO2 absolution rates comparable with the most significant uptake regions of the world's oceans. To achieve the project’s goal a two-pronged activity plan is proposed that will, on the one hand, synergize extant research programs through the coordination of efforts and, on the other hand, will fill the research gaps left by those programs by encouraging collaborative research. We will link the efforts of scientists, educators and program managers from Argentina, Brazil, Chile, Peru, Uruguay and the USA.

More info...

VOCES website

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BIoGeochemical cycles in the SOUTHern Ocean: Role within the Earth System (BIGSOUTH)

The BIGSOUTH project aims to achieve a detailed understanding of the processes controlling functioning and strength of the oceanic biological pump for representative key areas of the Southern Ocean, including open ocean and sea-ice covered areas, to upgrade present day assessments of the carbon sequestration capacity and nutrient cycling in the Southern Ocean and possible impacts on the global ocean. Therefore, we apply a unique combination of stable isotope (natural and spiked isotopic abundances), geochemical tracers, trace element and modeling tools to study the relevant biogeochemical processes and control factors (including Fe) acting on the fluxes of carbon and the two major macronutrients N and Si in the open and seasonally sea-ice covered water column.

More info...

BIGSOUTH website

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Report from an IMBER Endorsed Project

Population Outbreak of Marine Life (POMAL) - an IMBER-Japan Project

Hiroaki Saito1, Shin-ichi Uye2

1Fisheries Research Agency, Tohoku National Fisheries Research Institute, Shiogama, Japan, Email: hsaito@affrc.go.jp

2Hiroshima University, Higashi-Hiroshima, Japan, Email: suye@hiroshima-u.ac.jp

Human society is largely dependent on a stable supply of ecosystem services. Our expectation of stability is usually fulfilled by the intrinsic resilience of ecosystems to perturbation. However, ecosystems are never stable, and sometimes shift drastically from one state to another state if external forcings exceed a threshold. Unexpected changes still come as a “surprise” because of our limited understanding of the mechanisms of ecosystem change. Due to enhanced anthropogenic activities, unexpected ecosystem changes occur more frequently than before. Improving our understanding of the mechanisms of marine ecosystem responses to natural and/or anthropogenic forcings, and finding appropriate ways to use marine ecosystem services sustainably, are emergent issues in the global change era.

To this end, IMBER-Japan carried out the multidisciplinary research project POMAL (Population Outbreak of Marine Life) from 2007-2012, funded by the Ministry of Agriculture, Forestry and Fisheries of Japan. POMAL had two sub-projects: SUPRFISH (Studies on prediction and application of fish species alternation) and STOPJELLY (Studies on prediction and control of jellyfish outbreaks). The former focused on the mechanisms of pelagic fish species alternation, induced by natural climate change. It was carried out in the Kuroshio Extension region (KEX), where drastic change in SST and other physical properties in 1988/89 induced successive failure of the recruitment of Japanese sardine and subsequent increase of Japanese anchovy (Noto and Yasuda, 1999). STOPJELLY aimed to clarify the mechanisms of jellyfish blooms mainly in association with anthropogenic impacts. The moon jellyfish (Aurelia aurita) has bloomed more frequently and over a larger area in Japanese coastal waters in recent decades, and the giant jellyfish (Nemopilema nomurai) has bloomed in the Sea of Japan almost annually since 2002 (Uye, 2008), causing severe damage to local fisheries and power plant operations.

Research highlights from SUPRFISH

Fish species alternation (FSA) is considered to be a climate change driving event (Kawasaki, 1983). The last collapse of the Japanese sardine stock began in 1988 when winter SST and SSH anomalies (SSTa, SSHa) in the KEX increased dramatically. After 1988, recruitment of Japanese sardine continued to fall, despite historically high levels of egg production (>4x1015 eggs yr-1, 1988-1991), and the stock level decreased from 2x107 ton (1986) to <5x105 ton (early 2000s). Using a hindcast experiment by the eddy-resolving model OFES, it was elucidated that the North Pacific Gyre Oscillation index (NPGO; Di Lorenzo et al. 2008) preceded SSHa variability in the KEX by 3-4 years. Both OFES and linear Rossby wave models showed that Rossby wave-propagated high SSHa were present from the central North Pacific (1984) to the KEX (1988) (Fig. 11). High SSHa induced high SSTa and shallow winter mixed layer depth (WMLD) in the KEX for several years. The recruitment success of Japanese sardine was negatively correlated with SSTa, and positively correlated with WMLD (Nishikawa et al., 2011) (Fig. 12). An ecosystem model experiment showed that shallow WMLD induced early initiation of the spring phytoplankton bloom (Feb-Mar) at low magnitude, which resulted in a mismatch of prey zooplankton production and larval sardine arrival in the KEX (April-May) (Nishikawa et al., 2008). Nonaka et al. (2012) confirmed the 3-year advanced predictability of the Kuroshio Extension jet speed with the SSHa in the central North Pacific (r=0.68). Thus, the FSA in the KEX was potentially predictable by monitoring the SSHa in the central North Pacific.


Figure 11. Time-longitude section at 32°N of SSHa (13-month running mean).


Figure 12. Temporal variation of February MLD in the KEX (solid line) and the index of Japanese sardine recruitment success (recruitment per spawner biomass, broken line).

Research highlights from STOPJELLY

As most cnidarian jellyfish have a life cycle alternating a sexual pelagic medusa phase and an asexual benthic polyp phase, the behaviour of the latter phase is crucial to the medusa population size. Polyps of A. aurita are not found on natural rocky or pebbled surfaces, but densely populate the undersurface of artificial structures such as floating piers in port enclosures, where natural predators, such as nudibranchs, are rare. The polyps usually reproduce by budding, the rate of which increases with increased temperature and food supply (Han and Uye 2010). They can endure hypoxic conditions, which normally kill other animals, particularly as podocycsts – an encysted mass of polyp cells covered with chitinous lamella (Thein et al. 2012). These suggest that human activities such as nutrient loading, ocean warming and marine construction are advantageous for the enhancement of polyp population size in A. aurita. Polyps of N. nomurai reproduce only by means of podocyst production, and podocysts are capable of dormancy for at least six years. Excystment of the podocysts into active polyps is induced by exposure to hypoxia, followed by the return to aerobic conditions (Kawahara et al. 2013). This suggests that the spreading of the anoxic zone in Chinese waters, a seeding and nursery ground of this species, may be responsible for recent increases in the incidence of blooms. Since planktonic medusae and fish compete for zooplankton prey, and directly prey on each other, fish stock depletion by overfishing and/or hypoxia is also advantageous for jellyfish proliferation. Thus, jellyfish population outbreaks promote positive feedback loops under strong anthropogenic forcing, and the ecosystem transforms from a fish-dominated to a jellyfish-dominated system, i.e., “jellyfish spiral” (Uye, 2011) (Fig. 13).


Figure 13. Schematic representation of “jellyfish spiral’’.


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  • Han, C.-H. and Uye, S., 2010. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankton Benthos Res., 5: 98–105.
  • Thein, H., Ikeda, H. and Uye, S., 2012. The potential role of podocysts of the common jellyfish, Aurelia aurita s.l. (Cridaria: Scyphozoa) in anthropogenically perturbed coastal waters. Hydrobiologia 690: 157-167.
  • Kawahara, M., Ohtsu, K. and Uye, S., 2013. Bloom or non-bloom in the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae): roles of dormant podocysts. J. Plankton Res., 35: 213-217.
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 The Call for Abstracts for the IMBER Open Science Conference 2014 is open!

Theme: Future Oceans: Research for marine sustainability, multiple stressors, drivers, challenges and solutions

When and where: 23 - 27 June 2014 in Bergen, Norway

Who should come: Physical, natural and social sciences research communities interested in marine issues in the framework of global change and the transition towards marine sustainability


The IMBER Future Oceans conference will enable marine researchers and research end-users to share their knowledge and experience.

The ultimate goal is  to foster collaborative, interdisciplinary marine research that addresses human-natural marine science issues and to provide guidance for decision makers, managers and communities towards marine sustainability.


For more information please visit:IMBER OSC website

We look forward to seeing you in Bergen!

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6th China-Japan-Korea IMBER Symposium (3-4 October 2013, Tokyo, Japan)

You are invited to attend the 6th symposium organised by IMBER's very active research communities in China, Japan and Korea.

The symposium aims to:

  • advance understanding of marine biogeochemistry and ecosystem dynamics for the sustainable use of ecosystem services
  • better understand the response of various marine ecosystems to multi-stressors and drivers, from climate change to anthropogenic forcing.

Register (no registration fee!) and submit an abstract at:


Deadline for registration and abstract submission: 30 August 2013

 For more information, please see:6th CJK IMBER Symposium website

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  • Faming Li, Jingling Ren, Li Yan, Sumei Liu, Chenggang Liu, Feng Zhou and Jing Zhang. 2013. The biogeochemical behavior of dissolved aluminum in the southern Yellow Sea: influence of the spring phytoplankton bloom. Chinese Science Bulletin 58(2): 238-248. doi: 10.1007/s11434-012-5512-5. Article
  • Jun Sun, Yuanyuan Feng, Dan Wang, Shuquan Song, Yan Jiang, Changling Ding and Ying Wu. 2013. Bottom-up control of phytoplankton growth in spring blooms in Central Yellow Sea, China. Deep Sea Research Part II: Topical Studies in Oceanography  (In Press). doi: 10.1016/j.dsr2.2013.05.006. Article
  • Jun Sun, Yuanyuan Feng, Feng Zhou, Shuqun Song, Yan Jiang and Changlin Ding. 2013. Top-down control of spring surface phytoplankton blooms by microzooplankton in the Central Yellow Sea, China. Deep Sea Research Part II: Topical Studies in Oceanography (In Press). doi: 10.1016/j.dsr2.2013.05.005. Article
  • lan R. Jenkinson and Jun Sun. 2013. Drag increase and drag reduction found in phytoplankton and bacterial cultures in laminar flow: Are cell surfaces and EPS producing rheological thickening and a Lotus-leaf Effect? Deep Sea Research Part II: Topical Studies in Oceanography (In Press). doi: 10.1016/j.dsr2.2013.05. 028. Article
  • Li Zhao, Yuan Zhao, Wuchang Zhang, Feng Zhou, Cuixia Zhang, Jingling Ren, Xiaobo Ni, Michel Denis and Tian Xiao. 2013. Picoplankton distribution in different water masses of the East China Sea in autumn and winter. Chinese Journal of Oceanology and Limnology 31(2): 247-266. doi: 10.1007/s00343-013- 2085-3. Article
  • Lingfeng Huang, Shiquan Lin, Yuan Xiong, Jiachang Lu and Linnan Wu. 2013. Progress in the study of the selective feeding of heterotrophic nanoflagellate. Acta Oceanologica Sinica (in Chinese) 35(2): 1-8. Article
  • Mackenzie F. T. and Andersson A. J. 2013. The Marine Carbon System and Ocean Acidification during Phanerozoic Time. Geochemical Perspectives 2 (1):1-227. doi: 10.7185/geochempersp.2.1. Article
  • Min Liu, Yi Dong, Wuchang Zhang, Jun Sun, Feng Zhou, Chenggang Liu, Jingling Ren, Sshixiang Bao and Tian Xiao. 2013. Diversity of bacterial community during spring phytoplankton blooms in the central Yellow Sea. Canadian Journal of Microbiology 59(5): 324-332. doi: 10.1139/cjm-2012-0735. Article
  • Min Liu, Tian Xiao, Jun Sun, Hao Wei, Ying Wu, Yi Dong, Yuan Zhao and Wuchang Zhang. 2013. Bacterial community structures associated with a natural spring phytoplankton bloom in the Yellow Sea, China. Deep Sea Research Part II: Topical Studies in Oceanography (In Press). doi: 10.1016/j.dsr2.2013.05.016. Article
  • Shiquan Lin, Lingfeng Huang, Zhisheng Zhu and Xiaoyan Jia. 2013. Changes in size and trophic structure of the nanoflagellate assemblage in response to a spring phytoplankton bloom in the central Yellow Sea. Deep Sea Research Part II: Topical Studies in Oceanography (In Press). doi: 10.1016/j.dsr2.2013.05.017. Article
  • Silyakova A., Bellerby R. G. J., Schulz K. G., Czerny J., Tanaka T., Nondal G., Riebesell U., Engel A., De Lange T. & Ludvig A., 2013. Pelagic community production and carbon-nutrient stoichiometry under variable ocean acidification in an Arctic fjord. Biogeosciences 10: 4847-4859. Article
  • Smith B., Baron N., English C., Galindo H., Goldman E., McLeod K., Miner M. and Neeley E. 2013. COMPASS: Navigating the Rules of Scientific Engagement. PLoS Biol 11(4):e1001552. doi:10.1371/journal.pbio.1001552. Article
  • Suzuki T., Ishii M., Aoyama M., Christian J. R., Enyo K., Kawano T., Key R. M., Kosugi N., Kozyr A., Miller L. A., Murata A., Nakano T., Ono T., Saino T., Sasaki K., Sasano D., Takatani Y., Wakita M. and Sabine C. L. 2013. PACIFICA Data Synthesis Project. ORNL/CDIAC-159, NDP-092. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee. doi:10.3334/CDIAC/ OTG.PACIFICA_NDP092. Article
  • Takahashi T., Sutherland S.C. and Kozyr A. 2013. Global Ocean Surface Water Partial Pressure of CO2 Database: Measurements Performed During 1957-2012 (Version 2012). ORNL/CDIAC-160, NDP-088(V2012). Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee, doi: 10.3334/CDIAC/OTG.NDP088(V2012). Dataset
  • Ying Yu, Wuchang Zhang, Meiping Feng, Haibo Li, Yuan Zhao and Tian Xiao. 2013. Spatiotemporal distribution patterns of planktonic ciliates in the world sea areas. Chinese Journal of Ecology (in Chinese) 32(4): 1045-1053. Article 
  • Ying Yu, Wuchang Zhang, Shiwei Wang and Tian Xiao. 2013. Abundance and biomass of planktonic ciliates in the sea area around Zhangzi Island, Northern Yellow Sea. Acta Ecologica Sinica 33(1): 45-51. doi: 10.1016/j. chnaes.2012.12.007. Article
  • Ying Yu, Wuchang Zhang, Zengjie Jiang, Yuan Zhao, Meiping Feng, Haibo Li and Tian Xiao. 2013. Seasonal Variation of planktonic ciliates in sanggou Bay, Huanghai Sea. Acta Oceanologica Sinica (in Chinese) 35(3): 215-224. Article 
  • Yuan Zhao, Li Zhao, Tian Xiao, Chenggang Liu, Jun Sun, Feng Zhou, Sumei Liu and Lingfeng Huang. 2013. Temporal variation of picoplankton in the spring bloom of Yellow Sea, China. Deep Sea Research Part II: Topical Studies in Oceanography (In Press). doi: 10.1016/j.dsr2. 2013.05.015. Article
  •  Zhuoyi Zhu, Jing Zhang, Ying Wu, Yingying Zhang, Jing Lin and Qian Ji. 2013. Early degradation rate particulate organic carbon and phytoplankton pigments under differenct dissolved oxygen level off the Changjiang (Yangtze) river estuary. Oceanologia et Limbologia Sinica (in Chinese) 44(1): 1-8. Article
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ISSN 1951-610X