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Issue n°23 - April 2013

Issue n°23 - April 2013
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In this issue

Lisa Maddison

The first quarter of the year has been a busy time for IMBER. We kicked off with IMBIZO lll (28-31 January 2013) at the National Institute of Oceanography in Goa, India. By all accounts the meeting was a great success, with participants enjoying the science presented in the three concurrent workshops, and lively plenary discussions of over-arching questions that cut across all three workshop themes. The presentations from the three workshops are available on the IMBER website (http://www.imber.info/index.php/Meetings/IMBIZO/IMBIZO-III), and the next issue of the IMBER Update (to be published in July) will be dedicated to science highlights from the meeting.

Soon after IMBIZO lll, the IMBER regional programme CLIOTOP (Climate Impacts on Oceanic Top Predators), held its 2nd symposium at the Secretariat for the Pacific Community in Noumea, New Caledonia (11-15 February 2013). This is the main focus of the science highlights in this issue. The introductory article by the CLIOTOP Scientific Committee co-Chairs - Alistair Hobday and Kevin Weng - provides an overview of the symposium. The remaining articles highlight work carried out by some of the CLIOTOP working groups and other presenters.

Reports on GENUS (Geochemistry and Ecology of the Namibian Upwelling System) and AMT (Atlantic Meridional Transect) provide an update on activities in these two IMBER-endorsed projects.

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Science Highlights from CLIOTOP

The 2nd CLIOTOP symposium

Alistair Hobday and Kevin Weng (CLIOTOP co-Chairs)

The general objective of CLIOTOP is to facilitate a large-scale worldwide comparative effort aimed at identifying the impact of both climate variability (at various scales) and fishing on the structure and function of open ocean pelagic ecosystems and their top predator species, by elucidating the key processes involved in open ocean ecosystem functioning. The ultimate objective is the development of a reliable predictive capability for the dynamics of top predator populations and oceanic ecosystems that combines both fishing and climate (i.e. environmental) effects.

CLIOTOP, one of the four IMBER regional programmes, held its 2nd symposium in Noumea, on the Pacific island of New Caledonia, 11-15 February 2013. Known as the Pacific ‘French Rivera’, Noumea offered attendees a delightful conference venue. While science was foremost at the meeting, early sunrise and late sunset times allowed many to enjoy swimming and snorkeling at Anse Vata and Baie des Citrons.

The symposium was organized by an international committee and hosted by the Secretariat of the Pacific Community.


Figure 1. Organising committee for the 2nd CLIOTOP symposium: L to R: Karen Evans (CSIRO), Johann Bell (SPC), Christophe Menkes (IRD), Haritz Arrizabalaga (ATZI Tecnalia), Jock Young (CSIRO), Alistair Hobday (CSIRO), Lisa Maddison (IMBER), Joel Llopiz (WHOI), Kevin Weng (Univ. of Hawaii).

The second symposium made it clear that climate change is affecting the open ocean through interactions of stratification, deoxygenation, warming and acidification. The research spotlight has advanced from a focus on documenting impacts from individual climate stressors, to understanding the interactions of multiple changes, exploring socio-economic consequences, and in some cases, evaluating adaptation options that can reduce vulnerability to climate change. This is particularly relevant in the Pacific region where many Pacific islands and their communities are facing challenges associated with rising sea levels, higher intensities of cyclones and increasing demands for food security. One reason for holding the symposium in the Pacific was to increase focus on this region.

The overall objectives of the 2nd symposium were to:

  1. Review the effects of climate and climate variability on seasonal to decadal time scales on species, fisheries and dependent socio-economic and management systems;
  2. Review the current climate change impacts (including detection and attribution issues) and evaluate the impact of future climate change on pelagic species (prediction);
  3. Identify risk assessment or management evaluation tools that incorporate climate variability in order to improve sustainable resource management (conservation, fisheries, spatial planning) though adaptation initiatives.

Four of the six CLIOTOP working groups, and two cross-cutting topics were represented in presentations and posters at the symposium.

  • Working Group 1: The early life history dynamics of oceanic top predators are likely driven by a combination of density-dependent and -independent processes tightly linked to environmental processes. For example, changes in climate can impact ocean temperature distribution, timing and depth of stratification, and consequently primary production. Changes in production can directly influence rates of growth and mortality of early life history stages of top predators, either impacting their survival, or via migratory movements of the adults, the temporal and spatial distribution of spawning. Presentations on the early life history of pelagic species showed that improvements in data collection techniques were now generating additional insight into the fine scale behaviour and distribution of larval and juvenile fishes (see Fukuda article) and allowing for global comparisons. Early feeding behaviour was also critical to survival and new data for northern hemisphere cod showed the value of a comparative approach. Key gaps include understanding the behaviour of larval stages sufficiently to model their dispersal and transport accurately.
  • Working Group 2: Oceanic top predators (e.g., tunas, billfishes, sharks, birds, mammals, turtles) are highly adapted to exploit the pelagic environment and select specific locations depending on the dynamics of water masses, features and processes. The combination of animal tracking studies, oceanography and modeling are starting to yield an understanding of these species and projections of future distribution under a range of climate scenarios. Key gaps include understanding changes in behaviour and movement with ontogeny, and understanding movement and habitat selection and basin scales.
  • Working Group 3: Trophic pathways are changing in response to climate change and fisheries. There is growing evidence that climate variability affects primary producers in marine systems, imparting bottom-up forces on food webs via trophic pathways. Simultaneously, fisheries removals of upper-level predators can have cascading effects on the underlying trophic levels. Classical diet studies have provided most of the historical information on trophic pathways in pelagic ecosystems, but isotope and signature fatty acids are allowing new questions to be tested. The largest gap in our knowledge of trophic pathways in pelagic ecosystems remains the intermediate trophic levels - small fishes, cephalopods, and crustaceans. Several presentations showed how information on these mid-tropic species is being gathered using acoustic techniques, and estimates of biomass can then be used in ecosystem models. An important breakthrough, addressed by several presentations, was the use of regression tree analysis developed as part of CLIOTOP to analyse trophic relationships (an analysis package will soon to be available in R). (See Olson article)
  • Working Group 4: Synthesis and modelling efforts have focused on end to end ecosystem models including SEAPODYM, APECOSM and Atlantis. Managers have recently begun consulting these models to assess impacts of climate change on resources within key areas (such as EEZs or high seas pockets). Intermediate complexity and minimally realistic models were also illustrated at the symposium (see Melbourne-Thomas article). The objective of WG4, to develop multiple modeling approaches to identify a suite of potential ecosystem reference points that are pertinent to the management of oceanic fisheries, is now within reach, and comparing these multiple models will be a future focus.
  • Two cross-cutting themes were included in the symposium. The first considered pelagic conservation-fisheries management conflicts. Humanity is striving to balance food security, economic stability and growth, the health of key fish stocks, biodiversity conservation and ecosystem function. Climate change may make this balancing act more difficult, as the ranges and productivity of species change in time and space. A paper arising from the symposium will explore this topic.
  • The second theme asked if high resolution models are required to understand the ecology of climate change, and subsequently if low resolution global models are insufficient. These sessions included contributions from a number of physical oceanographers seeking to link their work to biological forecasts. 

In addition to contributed papers and posters, four keynote speakers addressed topics central to the goal of CLIOTOP (see Galvan-Magana article).


Figure 2. Keynote speakers at the 2nd CLIOTOP symposium (L to R): Olivier Maury, Felipe Galvan-Magana, Dan Costa, and John Hampton

Progress since the 1st CLIOTOP Symposium

There has been significant progress since the 1st Symposium (La Paz, Mexico 2007, www.confmanager.com/main.cfm?cid=722), with an expansion in the phyla considered, the geographic areas covered, and more sophisticated approaches being used. The “tropical tuna focus” of CLIOTOP expanded to temperate and polar regions where marine mammals and birds are key predators and groundfish, such as cod, are important. Many researchers are now using future climate scenarios to make projections for biological patterns of the future. The comparative approach, central to CLIOTOP, is also advancing, with global early life history analyses (WG 1), development of global prey and isotope databases (WG 3), and availability of projections from multiple ecosystem models (WG 4). Tool development to support comparative analyses has also advanced to include new approaches to assist statistical analysis, model fitting, and formulation of habitat models.


Figure 3. A Wordle comparison of words in the titles and abstracts of the presentations at the 1st and 2nd CLIOTOP symposia. Size of the word indicates the relative frequency of word use. The circles and lines indicate some differences between the word frequencies that indicate a change in emphasis.

With regard to the overall objectives of the symposium, some topics are clearly being addressed, while others require additional attention:

  1. The environmental habitat requirements of key species are now understood well enough to evaluate the impact of future climate change on pelagic ecosystems. Half the presentations addressed the effects of climate variability on species and fisheries over seasonal to decadal time scales. Additional effort to use a wider range of future climate scenarios to compare multiple biological model outputs will occur in coming years.
  2. Impacts on humans were not considered in most studies, so the inclusion of ourselves as apex predators in both data collection and modeling is critical.  
  3. Risk assessment and climate adaptation were not strong themes at the symposium. We must develop management evaluation tools that incorporate climate variability in order to improve resource management (conservation, fisheries, spatial planning). What was apparent is that adaptation initiatives include many existing management approaches for pelagic systems, and tuning them to evaluate future climate change is achievable in the near-term based on the body of work to date.

Several gaps and areas for future attention were noted.

  • Models to forecast future distribution of top predators assume they will behave and respond to environmental conditions as they do today. Some adaptation and evolution is expected, but collecting data to condition models (the easy part) will be difficult.
  • The biology of a species may vary regionally, and such diversity may allow adaptation to future scenarios.  
  • Ensemble approach: just as the physical climate modelling community is using multiple climate models, so must biologists begin to compare outputs and forecasts from different ecosystem models, and consider selection of multiple GCMs in forcing the biological models. Consideration of the effects of resolution in models is also essential, as model structure influences model behaviour.

Awards, publications and future meetings

The best oral presentation by an early career researcher was awarded to Dr Jessica Melbourne-Thomas (Fig. 4), for her presentation Pelagic food web structure and function in the Southern Ocean: a comparative analysis – see article in this newsletter. The best poster award was presented to Vicki Hamilton (Fig. 5) from the University of Tasmania, for her poster titled Energetic variability in toothed whales and relationships with a changing marine environment.

Olivier Maury, who initiated CLIOTOP with Patrick Lehodey in 2001 and served as the co-chair for 10 years, has stepped down as co-chair. Olivier has served the community tirelessly over the past decade, and we are very pleased that he will continue to contribute as a member of the CLIOTOP Scientific Steering Committee.

A special issue of Deep Sea Research will publish papers from the symposium, and submissions are being prepared by many attendees. It is particularly pleasing to see that several papers are also being prepared as a result of discussions arising from the symposium sessions.

The 3rd CLIOTOP symposium is scheduled for June 2015, most probably at a venue in western Europe.

Thanks to the sponsors

The financial support of the symposium sponsors was critical and allowed us to attract an international group to New Caledonia, and to host several social functions during the meeting. Particularly, we acknowledge the support of AZTI Tecnalia, Collecte Localisation Satellites (CLS), CSIRO, IMBER, the Institut de Recherche pour le Développement (IRD), the Pacific-Australia Climate Change Science and Adaptation Planning program (PACCSAP) and the Secretariat of the Pacific Community (SPC).


Figure 4. Jess Melbourne-Thomas receives the award for the best oral presentation by an early career scientist from Kevin Weng (CLIOTOP Co-Chair)


Figure 5. Joel Llopez (CLIOTOP SSC member) presents Vicki Hamilton with the award for the best poster presentation

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Schooling behaviour of Pacific bluefin tuna during the first year of their life

H. Fukuda1, S. Torisawa2, T. Takagi2, K. Fujioka1, H. Mitamura3, K. Ichikawa4, N. Arai3, and Y. Takeuchi1

1National Research Institute for Far Seas Fisheries, 5-7-1 Orido, Shimizu, Shizuoka 424-0902, JAPAN

2Faculty of Agriculture, Kinki University, 3327-204 Naka-machi, Nara 631-8505, JAPAN

3Graduate School of Informatics, Kyoto University, 36-1 Yoshida-Honmachi, Sakyo-ku, Kyoto 606-8501, JAPAN

4Research Institute for Humanity and Nature, National Institutes for the Humanities, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, JAPAN



‘The tunny proper, the pelamys, and the bonito penetrate into the Euxine in summer and pass the summer there; as do also the greater part of such fish as swim in shoals with the currents, or congregate in shoals together. And most fish congregate in shoals, and shoal-fishes in all cases have leaders’.

As Aristotle mentioned in ‘The History of Animals’ (above), shoaling behaviour is a common form of social aggregation among teleosts and is considered to render ecological benefits, such as reduced predation risks and improved foraging (Pitcher & Parrish, 1993). More than two thousand years after he described the migration and shoaling behaviour of tuna-like species, we are still attempting to understand the migration of tuna shoals more precisely.

The term ‘schooling’ differs from ‘shoaling’; the former shows directionally and temporally syntonic swimming of fish (polarized swimming), and the latter is just a cluster of fish without polarized swimming. In this study we investigated the ontogeny of schooling behaviour of Pacific bluefin tuna, Thunnus orientalis, during their early life history. We also observed schooling behaviour of 1.5 year-old T. orientalis (around 70 cm in body length [BL]) in a sea net cage, using a new biotelemetry technique, and introduce a new methodology to observe their schooling behaviour.



Figure 6. Changes in the index of parallel swimming with neighbouring fish (Separation swimming index; Nakayama et al., 2001). Lower value indicates parallel swimming with neighbours. The dotted line indicates the expected value (1.27) for randomly swimming fish. Asterisks below the bars indicate that the value is significantly smaller than the expected value for randomly swimming (1.27).


Figure 7. Changes in mean swimming speeds.


Schooling behaviour in the early life history

It was found that T. orientalis started to form schools about 25 days after hatching (Fig. 6). At that time, they had a BL of about 2-3 cm, which coincides with the completion of metamorphosis from larva to juvenile. Developmental changes in the swimming organs, sensory organs, and central nervous system during metamorphosis enhance the ability of T. orientalis to swim in a synchronized manner with neighbours (Fukuda et al., 2010).

T. orientalis suffer high mortality during the first two weeks after hatching due to starvation and starvation-induced predation (Tanaka et al., 2006; Tanaka et al., 2008). The onset of schooling occurs quite a while after this critical period in this species. Juveniles may prioritize foraging over schooling during the high mortality period, in order to enhance growth and avoid starvation. After the critical period, rapid improvement in swimming ability was observed (Fig. 7). The juveniles exhibited highly polarized swimming, ensuring that they remained in a group (Fig. 6). Schooling may be advantageous for the survivors during this high mortality period, as they begin to migrate in fast-moving schools.

A new technique to observe schooling behaviour

Most quantitative estimations of schooling behaviour (including this one), were based on visual observations using a video camera. The experiments were typically carried out in a water tank, which consequently resulted in spatial limitations. To overcome this constraint, we used a fine-scale acoustic positioning and telemetry system, to obtain swimming trajectories of tuna in an outdoor net cage. The Automatic Underwater SOund Monitoring System version 3.0 (AUSOMS) (Aquasound Inc., Kyoto, JAPAN), can record full frequency bands of underwater sound in stereo (Shinke et al., 2011).

Three AUSOMSs installed along the rim of a 10m2 net cage (6 m deep) determined the position of the plural ultrasonic transmitters, attached to the backs of 1.5-year-old T. orientalis (Fig. 8a). Each transmitter has a pressure sensor, and emits a different frequency band (57-83 kHz) every 1-2 seconds, depending on the depth. The position of each transmitter was determined by the difference in arrival time of the sound in the stereo hydrophones of each AUSOMS. From this, we obtained a 3-dimensional coordinate data time-series of T. orientalis swimming in the net cage (Fig. 8b). At this stage, direct comparisons of behavioural traits in 1.5-year-old and early life tuna are difficult due to the difference in observation methodologies. However, 1.5-year-old T. orientalis seem to form similar or, alternatively, looser schools as 55 day-old fish. Traits of schooling in both ages might not reflect the function to form polarized schools, but rather the necessity to school.


Figure 8. Schema of the experimental set-up from above the net cage (a). The white cylinders are the AUSOMSs version 3.0 on the rim of the net cage, and the black cylinders in the corners are the hydrophones. In (b), the swimming trajectories of three individuals during 23 seconds are shown.



  • Aristotle, 384-322 BC. The History of Animals. Translated by D’Arcy Wentworth Thompson, eBooks@Adelaide, The University of Adelaide Library.
  • Fukuda, H., Torisawa, S., Sawada, Y. and Takagi, T., 2010. Ontogenetic changes in schooling behaviour during larval and early juvenile stages of Pacific Bluefin tuna Thunnus orientalis. Journal of Fish Biology 76(7), 1841-1847.
  • Pitcher, T. J. and Parrish, J. K., 1993, Function of shoaling behaviour in teleosts. In: Pitcher T.J. (ed) Behaviour of teleost fishes, 2nd Edition, Chapman & Hall, New York, 363–439.
  • Shinke, T., Kamoshida, T., Ichikawa, K., Mitamura, H. and Arai, N., 2011. Development of a fine-scale acoustic positioning and telemetry system.
  • Tanaka, Y., Satoh, K., Iwahashi, M. and Yamada, H., 2006. Growth-dependent recruitment of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean. Marine Ecology Progress Series 319, 225–235.
  • Tanaka, Y., Satoh, K., Yamada, H., Takebe, T., Nikaido, H. and Shiozawa, S., 2008. Assessment of the nutritional status of field-caught larval Pacific bluefin tuna by RNA/DNA ratio based on a starvation experiment of hatchery-reared fish. Journal of Experimental Marine Biology and Ecology 354, 56–64.
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Are pelagic food webs changing in the eastern tropical Pacific Ocean? Ask the tuna

Robert J. Olson1, Leanne M. Duffy1, Petra M. Kuhnert2, Felipe Galván-Magaña3, Vanessa Alatorre-Ramírez3 and Noemi Bocanegra-Castillo4

1Inter-American Tropical Tuna Commission, 8604 La Jolla Shores Drive, La Jolla California 92037, USA

2CSIRO Mathematics, Informatics and Statistics, Private Bag 2, Glen Osmond SA 5064, Australia

3Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Apartado Postal 592, La Paz, Baja California Sur, C.P. 23000 México

4Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, C.P. 23096 México


Marine ecologists are challenged by questions about the implications of climate- and fisheries-induced ecosystem changes. Long-term changes in the oceans are beginning to alter the food webs in tropical and subtropical oceans, but the effects on mid-trophic level micronekton communities that support commercially-important pelagic fishes remain unclear.

Ecosystem changes are occurring on a scale seen to be capable of affecting prey communities. Primary production has declined over vast oceanic regions in recent decade(s) (Behrenfeld et al. 2006, Polovina et al. 2008, Stramma et al. 2008, Polovina and Woodworth 2012). In the North and South Pacific, oligotrophic surface waters have increased in area by 2.2 and 1.4 % yr-1 between 1998 and 2006, respectively, concurrently with significant increases in mean SSTs (Polovina et al. 2008).

Evidence is also strong that primary producers have changed in community composition and size structure in recent decades. Phytoplankton cell size is relevant to predation dynamics of pelagic fishes because food webs that have small picophytoplankton at their base require more trophic steps to reach predators of a given size than do food webs that begin with larger phytoplankton (e.g. diatoms), affecting energy transfer to the upper trophic levels (Seki and Polovina 2001). Barnes et al. (2010) developed a relationship to estimate the size composition of primary producers from environmental variables, and Polovina and Woodworth (2012) applied the Barnes et al. relationship to estimate monthly size compositions of phytoplankton communities in the subtropical oceans and the Pacific equatorial upwelling region during 1998-2007. With the seasonal component removed, the median phytoplankton cell size estimated for the subtropical North and South Pacific declined by 2.2% and 2.3%, respectively, over the 9-year period. 

  As expected, the classification tree revealed major diet differences due to the regional zoogeography of prey communities, but these were prominent only in relatively small subtropical regions in the extreme north and extreme south of the sample distribution (Fig. 9, grey circles on map). One of the most important splits in the tree, however, revealed that the bulk of the stomach samples over most of the ETP (“central region” 6°S–17°N, coast–150°W, Fig. 9, blue and red circles) were best explained by decadal sampling period, 1992-1994 and 2003-2005. Epipelagic fishes, including frigate and bullet tunas Auxis spp., declined from 82% to 31% of the diet by biomass in the central region over the decade (Fig. 9, bar plot). Auxis thazard and A. rochei were previously known to be abundant (Olson and Boggs 1986), and important prey species for much of the apex predator guild in the ETP (Olson and Watters 2003, Hunsicker et al. 2012). Earlier in the development of the purse-seine fishery (1970-1972), Auxis spp. comprised about 53% of the yellowfin tuna diet in a comparable central part of the ETP (Olson and Boggs 1986), declining to 34% in 1992-1994 and to 16% in 2003-2005 (Fig. 9). Mesopelagic fishes and squids increased from 9% to 29% of the diet over the decade, and an abundant crustacean, red crabs Pleuroncodes planipes, apparently expanded its distribution offshore and to the south, changing from <0.01% to 27% of the diet in the central region. Additionally, prey:predator size ratios showed that larger prey were consumed during 1992-1994 than during 2003-2005. Smaller prey, in general, occupy lower trophic levels than larger prey, and our results imply that yellowfin were feeding at lower trophic positions during the early 2000s than the early 1990s.

Figure 9. Details of splits of the 1 SE classification tree, showing sample locations, sample numbers, and prey compositions for 1811 yellowfin tuna at node 7 partitioned by sample period (1992-94 vs. 2003-05) into nodes 14 and 15. D is the gini index of diversity.

Expansion of the oxygen minimum zone (OMZ) also has consequences for prey communities and their predators. Time series of dissolved oxygen concentration at depth, from 1960 to 2008, revealed a vertical expansion and intensification of the OMZ in the central and eastern tropical Pacific and Atlantic, and in other regions of the world’s oceans (Stramma et al. 2008), resulting in a constricted epipelagic zone. For the epipelagic tunas and other large fishes, habitat compression restricts their depth distribution into a narrower surface layer, compressing their foraging habitat and altering forage communities (Stramma et al. 2012).

The mechanisms linking climate forcing to changes in food webs are not clear, and hence comparative and observational approaches using historical data are required (Francis and Hare 1994). In a recent study, we examined broad-scale spatial, temporal, environmental, and biological relationships with predator-prey data for yellowfin tuna (Thunnus albacares) in the eastern tropical Pacific using a modified classification tree approach developed for diet data by Kuhnert et al. (2012). One of the objectives was to examine the degree and scale of diet variability on a decadal time frame. We analyzed the diet composition of yellowfin based on 6810 samples from 433 purse-seine sets on 212 fishing trips during two 2-year periods separated by a decade. The samples were taken over the entire region of operation of the eastern Pacific tuna purse-seine fishery (Fig. 9) during 1992-1994 and 2003-2005. Hence, observed trends in yellowfin prey composition were considered indicative of changes in prey communities over the majority of the sample region.


In summary, a novel classification and regression tree methodology revealed that a major diet shift had transpired in the heart of the ETP during the decade between the early 1990s and early 2000s. Altered prey composition and patterns suggest that broad-scale changes in the pelagic food web had occurred in the ETP. Circumstantial evidence of simultaneous broad-scale reductions in biological production and phytoplankton size composition, and a vertical expansion of the hypoxic oxygen minimum zone in the central and eastern tropical Pacific, point to ecosystem change on a scale capable of altering prey communities. However, no fisheries-independent evidence of changing prey abundance is available for comparison with yellowfin diet trends. Until new methods are developed (see CLIOTOP’s MAAS project, (Handegard et al. 2012), we advocate that low-level, systematic sampling programs of stomach contents from yellowfin or other pelagic fishes be adopted for continuous monitoring of mid-trophic level communities in pelagic ecosystems (Nicol et al. 2013).


We acknowledge the contribution of the IMBER regional programme CLIOTOP, via workshops of CLIOTOP Working Group 3 to the development of some of the ideas and methods in this article.



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Modelling foodweb responses to harvesting and climate change in different regions of the Southern Ocean

Jess Melbourne-Thomas1,2 and Andrew Constable1,2

1Australian Antarctic Division, Channel Highway, Kingston, Tasmania 7050 Australia

2Antarctic Climate and Ecosystems Cooperative Research Centre, Private Bag 80, Hobart Tasmania 7001, Australia


Southern Ocean ecosystems play an important role in global biogeochemical cycles and can act as “sentinels” for understanding and predicting the effects of climate change on marine ecosystems globally. However, there is still a high degree of uncertainty regarding the function and resilience of marine foodwebs in many regions of the Southern Ocean. Climate change responses of higher predators, notably whales and penguins, in Southern Ocean foodwebs will be influenced by change in physical habitats combined with the responses of phytoplankton and zooplankton species to those changes. Management of Antarctic fisheries will need to account for these changes in order to remain sustainable. While foodweb structure has been documented and modelled for particular, well-studied regions of the Southern Ocean there has been no circumpolar analysis of similarities and differences in foodweb operation between these regions, and the consequent responses of higher predators. Nor has there been a comparative assessment of responses related to the introduction and expansion of krill fisheries to those regions.

We implemented network models for foodwebs in the four Southern Ocean regions based on recently developed trophic models for the Scotia Sea, the West Antarctic Peninsula and the Ross Sea (Hill et al. 2012, Murphy et al. 2013, Pinkerton et al. 2010). Some modifications were made to these models to achieve consistency in the level of detail for functional group representations across regions. The model for East Antarctica was based on a literature search and expert opinion regarding the nature of trophic linkages in this region. We thenrepresented the effects of harvesting and climate change in each model as a series of drivers that have direct effects on specific trophic groups. For climate change, we focused on the potential effects of temperature, acidification, nutrient availability, wind strength, variability in the location of frontal features, and the extent and duration of sea ice.

Foodweb model development

We used a qualitative network modelling approach (Melbourne-Thomas et al. 2012, 2013) to compare foodweb characteristics and marine ecosystem function between four major regions of the Southern Ocean: (1) the Scotia Sea, (2) East Antarctica, (3) the Ross Sea, and (4) the West Antarctic Peninsula (Fig. 10). Two key advantages of this approach are the ability to capture feedback effects, and to easily assess differences in foodweb-level responses to perturbation in the face of uncertainty. The method also facilitates identification of key foodweb linkages that affect system responses to disturbance and stress. Because qualitative models only represent the direction, not the magnitude, of interactions they provide a relatively quick and simple way to explore the nature of system-level responses to change, without the need for detailed parameterisations.

We implemented network models for foodwebs in the four Southern Ocean regions based on recently developed trophic models for the Scotia Sea, the West Antarctic Peninsula and the Ross Sea (Hill et al. 2012, Murphy et al. 2013, Pinkerton et al. 2010). Some modifications were made to these models to achieve consistency in the level of detail for functional group representations across regions. The model for East Antarctica was based on a literature search and expert opinion regarding the nature of trophic linkages in this region. We then represented the effects of harvesting and climate change in each model as a series of drivers that have direct effects on specific trophic groups. For climate change, we focused on the potential effects of temperature, acidification, nutrient availability, wind strength, variability in the location of frontal features, and the extent and duration of sea ice.


Figure 10. Qualitative network models were developed for pelagic foodwebs in four regions of the Southern Ocean, based on current knowledge of trophic linkages and key functional groups for each region (Hill et al. 2012, Murphy et al. 2013, Pinkerton et al. 2010).

Perturbation scenarios and regional responses

We examined the qualitative responses of our foodweb models to three scenarios: (1) an increase in harvesting, (2) climate change, and (3) a combination of increased harvesting and climate change. We perturbed climate change variables in the direction that is expected in the future, and considered uncertainty associated with the interactions between these variables (e.g. the effects of acidification and wind strength on nutrient availability). System-level responses to these perturbation scenarios were visualised using multivariate ordination (principal components analysis).

Changes in regional foodwebs were dominated by the effects of climate change, and were characterised by decreases in phytoplankton and zooplankton (Fig. 11). Notably, the nature of foodweb responses to climate change was consistent across our four modelled regions. However, under an increase in harvesting alone (without climate change effects), we saw much more pronounced variability in foodweb responses across regions. This variability was associated with differences in the responses of krill and of demersal fish.

Simple modelling approaches such as the one demonstrated here can provide valuable information regarding the representation of foodwebs and environmental drivers in more complex, quantitative models. Comparative approaches such as ours might also usefully be applied to address questions regarding pelagic foodweb structure and function for other marine systems that are subject to the effects of fishing and climate-related environmental change.


Figure 11. Principal components ordination of foodweb-level responses for the four modelled regions under three scenarios: (1) an increase in harvesting (black), (2) climate change (orange), and (3) both harvesting and climate change (brown). The analysis is based on the proportion of positive responses for all modelled groups under the three scenarios. Eigenvectors representing the association of particular model variables with the ordination axes are shown in the centre of the plot.



  • Hill, S. L., K. Keeble, A. Atkinson and E. J. Murphy. 2012. A foodweb model to explore uncertainties in the South Georgia shelf pelagic ecosystem. Deep Sea Research Part II: Topical Studies in Oceanography 59-60:237–252.
  • Melbourne-Thomas, J., S. Wotherspoon, B. Raymond and A. Constable. 2012. Comprehensive evaluation of model uncertainty in qualitative network analyses. Ecological Monographs 82:505–519.
  • Melbourne-Thomas, J., A. Constable, S. Wotherspoon and B. Raymond. 2013. Testing paradigms of ecosystem change under climate warming in Antarctica. PLoS ONE 8:e55093.
  • Murphy, E. J., E. E. Hofmann, J. L. Watkins, N. M. Johnston, A. Piñones, T. Ballerini, S. L. Hill, P. N. Trathan, G. A. Tarling, R. A. Cavanagh, E. F. Young, S. E. Thorpe and P. Fretwell. 2013. Comparison of the structure and function of Southern Ocean regional ecosystems: The Antarctic Peninsula and South Georgia. Journal of Marine Systems 109-110:22–42.
  • Pinkerton, M. H., J. M. Bradford-Grieve and S. M. Hanchet. 2010. A balanced model of the food web of the Ross Sea, Antarctica. CCAMLR Science 17:1–31.
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Felipe Galván-Magaña1, Ofelia Escobar-Sánchez2, Angélica María Barrera-García3, Carlos Julio Polo-Silva4,6 & Yassir Eden Torres-Rojas5 

1Centro Interdisciplinario de Ciencias Marinas. Instituto Politécnico Nacional. Apdo. Postal 592. La Paz, Baja California Sur, México.

2Instituto Tecnológico de Mazatlán. Calle Corsario No. 203. Col. Urias. C.P. 82070, A.P. 757, Mazatlán, Sinaloa

3Centro de Investigaciones Biológicas del Noroeste. Mar Bermejo 195.Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur. C.P. 23090

4Oficina de Generación del Conocimiento y la Información. Autoridad Nacional de Acuicultura y Pesca, Bogotá, Colombia.

5Instituto de Ciencias del Mar y Limnología. UNAM. Av. Joel Montes Camarena S/N
 Apartado Postal 811 C.P. 82040, Mazatlán, Sin. México

6Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apdo. Postal 70–305 Ciudad Universitaria, 04510 México, D.F., México.

Corresponding author: Felipe Galván-Magaña: galvan.felipe@gmail.com; fgalvan@ipn.mx

High trophic level marine animals including sharks, billfish, tuna and marine mammals are susceptible to the bioaccumulation of high concentrations of pollutants such as trace elements and Persistent Organic Pollutants (POPs, e.g., pesticides) (Cornish et al. 1997). This vulnerability has resulted in top predators being used as bioindicators of environmental pollution from heavy metals and organochlorines (Vas 1991, Marcovecchio et al. 1991; Storelli and Marcotrigiano 2001).

Several shark species are top predators and can bioaccumulate trace elements, such as mercury, in concentrations above the legal limit for human consumption in countries such as the United States (Davis et al. 2002) and Mexico (Barrera-García et al. 2012)

Top predators that feed on prey from different habitats (coastal, oceanic, benthic, and pelagic) can also be bioindicators of changes that occur in ecosystems through time. The generalist/opportunistic feeding behaviour of top predators, such as sharks (Ellis and Musick 2007) can reveal alterations in the trophic structure, as well as the impact of a decrease or absence of these predators, as a result of anthropogenic activities such as fishing.

Top predators as bioindicators of ecosystem changes

In the last 50 years, fishing pressure has increased in all the oceans, often resulting in a rapid decrease of communities with large predators (Myers and Worm 2003). Top predators play an important role in trophic chain structure and functioning in marine ecosystems (Stevens et al. 2000), and the decrease of these predators could have serious ecological consequences (Baum and Myers 2004; Shepherd and Myers 2005).

Galván-Magaña et al. (1989) carried out a study of the feeding habits of sharks in the Gulf of California, Mexico. The diet of the hammerhead shark Sphyrna zygaena was found to consist mainly of the cephalopods Onychoteuthis banksii and Histioteuthis heteropsis, and squid from the Cranchidae family. Twenty years later, S. zygaena in the same area consumed mostly the giant squid Dosidicus gigas (Ochoa 2009). This change in prey was probably caused by the overexploitation of sharks in the Gulf of California; because of reduced predation, D. gigas populations increased, and extended their distribution towards the northern Pacific (Zeidberg and Robison 2007).

The elimination of top predators and consequent increase in prey abundance can cause a cascade of indirect effects at several levels of the trophic web (Baum and Myers 2004; Schindler et al. 2002; Myers et al. 2007). In the North Atlantic, for example, the reduction of large predators resulted in an increase in the population of cownose rays (Rhinoptera bonasus), which feed mainly on clams (Argopecten irradians). Consequently, clam abundance decreased, resulting in the collapse of the clam fishery (Myers et al. 2007). The absence of sharks from areas where records show they were previously captured, indicates that there has been an alteration in the ecosystem.

In the Mediterranean Sea, the number of large sharks has decreased drastically in the past two centuries. Five of 20 recorded species have decreased from >96 to 99.99%, which classifies them as endangered species, according to the International Union for the Conservation of Nature (IUCN). It has been noted that after shark overexploitation, there is no rapid population recovery; so, not only these predators feel the ecological impact - it is also felt at the ecosystem level.

Dambacher et al. (2010) analyzed the diets of top predators in three regions of the Pacific Ocean to identify the key prey species in each trophic web, to use them as indicators of climate change perturbations (water warming), and to observe changes in the diversity of prey species they consumed. Top predators were used as bioindicators of changes in the ecosystem due to anthropogenic effects (fisheries), or to natural changes in the ecosystem (water warming, diminishing oxygen minimum layer, etc.).

Top predators as bio-indicators of pollutants

The marine environment is facing environmental problems due to both natural and human-induced impacts. Toxic substances discharged from agricultural and mining activities, of which the most important are pesticides, hydrocarbons and heavy metals, are the main culprits (Moreno et al. 1984; Bañuelos-Vargas 2007). The levels of these substances have risen to the extent that the health and the ecology of the ecosystems are at risk. Impacts include: degradation and loss of habitats, perturbations in biogeochemical cycles, and adverse effects on development, health and survival of organisms. Abnormalities in development, delayed growth, inhibition of reproduction, mortality at early life stages, ulcers, tumours, asphyxia, etc. have been observed (Kennish 2001); they reduce survival probabilities and therefore, the abundance of species.


Generally, in the marine environment, coastal and estuarine zones are considered to be more polluted due to their proximity to inhabited and manufacturing areas. As a result, the species that inhabit these areas are more exposed to toxic agents (Moreno et al. 1984). However, several shark species that live away from coastal areas have been found to have very high levels of toxic substances. For example, off the west coast of Baja California Sur, Mexico, an area considered pristine, mercury levels in the muscle of some sharks and blue marlin (Fig. 12) are above the international standards (FDS) set for human consumption (1.0 mg g-1 wet weight) (Escobar-Sánchez et al. 2011; Barrera-García et al. 2012, 2013; Maz-Courrau et al. 2012).


Figure 12. Mercury levels in top predators in Baja California Sur (Sphyrna zygaena, Prionace glauca, Isurus oxyrinchus, Alopias pelagicus, Carcharhinus limbatus, Kajikia audax, Coryphaena hippurus, Thunnus albacares, Makaira nigricans). The red line represents the permitted level for consumption by humans.

Although primary producers and organisms at the base of the food chain (molluscs, crustaceans) are considered good bioindicators of pollution in marine ecosystems, high trophic consumers (e.g., sharks, billfish, tuna, etc.) represent an important link to humans, as they are economically important species that could transfer harmful substances to humans. The concentration of substances in these top predators can therefore, provide information about which pollutants are present in a particular part of the ocean, and at what levels.

Although most sharks are migratory, some species do not migrate far. Coastal species of the genus Mustelus spp. and the angel shark Squatina californica are considered good indicators for the region. However, oceanic species that would be expected experience less anthropogenic influence should not be excluded. Young blacktip sharks (Carcharhinus limbatus), were found to have accumulated mercury transferred from the mother during gestation (Adams and McMichael 1999).

Sharks are long-lived species and so could function as indicators at longer time scales of bioaccumulation in the environment, mainly of pollutants with long-term effects (e.g., heavy metals).

After mercury exposure, darkening of the liver and neurological damage were observed in some sharks, such as Centrophorus granulosus (Hornung et al., 1993). Although levels above 1.0 mg g-1 (Ruelas-Inzunza and Paez-Osuna 2005) have been reported for several shark species (Sphyrna lewini, S. zygaena, Alopias pelagicus), the effects of these high levels were not apparent, and the animals are able to tolerate them. This could be due to elimination or detoxification mechanisms that allow certain species to live and reproduce in polluted environments where others are not able to.

Origin of pollutants

Pollutants from different anthropogenic sources enter the ocean via effluent and fluvial systems, atmospheric deposition and subterranean waters (Cope 2004; Erickson et al. 2008). Once in the ocean, they are distributed in the water column and sediments by physical, chemical and biological processes, and marine organisms come into contact with them via their gills and by feeding (Cope 2004; Erickson et al. 2008). The increase in trace elements in coastal fish is due to pollution from drainage discharges and industrial waste (Chan 1995).

Marine pollutants include trace elements and pesticides, which affect human health through the consumption of food of marine origin. Pesticides are anthropogenic pollutants such as organoclorides (e.g., DDT, aldrin), organophosphates (malathion), carbamates, and polychlorinated biphenyls (PCBs), that were introduced in the 70s (Cope 2004). They can cause alterations of the nervous and reproductive systems in marine organisms and in humans (de Azevedo e Silva et al. 2007; Storelli et al. 2005). Lead, arsenic, mercury, cadmium and even some elements like iron, copper and zinc that are essential for life can be toxic to humans if present in high concentrations. (Caurant et al. 2006; Cope 2004). Arsenic is found in different chemical forms in water, and if consumed can cause physiological alterations and even cancer in humans (Cope 2004; Ventura-Lima et al. 2011). Pollution by cadmium in marine organisms originates from electric plants and batteries among other sources (Betka y Callard 1999). Cephalopods tend to accumulate large concentrations of this element in their digestive glands, turning these organisms into cadmium transference vectors for top predators (Bustamante et al. 2002).

Mercury can be rapidly incorporated in the trophic chain as it is rapidly transformed by bacteria into methyl mercury (MeHg). This accumulates in the muscles of fish such as tuna, billfish and sharks (Barrera-García et al. 2012, 2013; Escobar-Sánchez et al. 2011), in which approximately 95% of mercury is found in its most toxic form, methyl mercury (Bloom 1992; Storelli et al. 2002).

In short, sharks are ecosystem health indicators as they consume prey from different habitats, and indicate their prey´s level of pollution, which can bioaccumulate in sharks´ tissues. Their high feeding rates and speed make them effective bioindicators of ecosystem changes, and enable us to distinguish changes in prey diversity due to environmental changes, from those due to the effect of reduced predation caused by overfishing.



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  • Bañuelos-Vargas, M. I. 2007. Concentración de metales pesados en el tejido blando de Crassostrea corteziensis de cuatro lagunas costeras del sur de Sinaloa, durante un ciclo anual. Tesis de Licenciatura. Facultad de Ciencias del Mar. Universidad Autónoma de Sinaloa.
  • Barrera-García, A., T. O´Hara, F. Galván-Magaña, L. C. Méndez-Rodríguez, J. M. Castellini, and T. Zenteno-Savín. 2012. Oxidative stress indicators and trace elements in the blue shark (Prionace glauca) off the east coast of the Mexican Pacific Ocean. Comparative Biochemistry and Physiology, Part C 156: 59–66.
  • Barrera-García, A., T. O’Hara, F. Galván-Magaña, L.C. Méndez-Rodríguez, J.M. Castellini, and T. Zenteno-Savín, 2013. Trace elements and oxidative stress indicators in liver and kidney of the blue shark (Prionace glauca). Comparative Biochemistry and Physiology. Part C. En prensa.
  • Baum, J. K. and R. A. Myers. 2004. Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7:135–145.
  • Betka, M. and G. V. Callard. 1999. Stage-dependent accumulation of cadmium and induction of metallothionein-like binding activity in the testis of the dogfish shark, Squalus acanthias. Biology of Reproduction 60:14-22.
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  • Bustamante, P., R. P. Cosson, I. Gallien, F. Caurant, and P. Miramand. 2002. Cadmium detoxification processes in the digestive gland of cephalopods in relation to accumulated cadmium concentrations. Marine Environmental Research 53:227-241.
  • Caurant, F., A. Aubail, V. Lahaye, O. Van Canneyt, E. Rogan, A. López, M. Addink, C. Churlaud, M. Robert, and P. Bustamante. 2006. Lead contamination of small cetaceans in European waters – The use of stable isotopes for identifying the sources of lead exposure. Marine Environmental Research 62:131-148.
  • Chan, K. M. 1995. Concentrations of copper, zinc, cadmium and lead in rabbitfish (Siganus oramin) collected in Victoria Harbour, Hong Kong. Marine Pollution Bulletin 31:277-280.
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  • Cornish, A. S., W. C. Ng, V. C. M. Ho, H. L. Wong, J. C. W. Lam, P. K. S. Lam, and K. M. Y. Leung. 2007. Trace metals and organochlorines in the bamboo shark Chiloscyllium plagiosum from the southern waters of Hong Kong, China. Science of the Total Environment 376:335-345.
  • Davis, J. A., M. D. May, B. K. Greenfield, R. Fairey, C. Roberts, G. Ichikawa, M. S. Stoelting, J. S. Becker and R. S. Tjeerdema. 2002. Contaminant concentrations in sport fish from San Francisco Bay, 1997. Marine Pollution Bulletin 44:1117-1129.
  • de Azevedo e Silva, C. E., A. Azeredo, J. Lailson-Brito, J. P. M. Torres and O. Malm. 2007. Polychlorinated biphenyls and DDT in swordfish (Xiphias gladius) and blue shark (Prionace glauca) from Brazilian coast. Chemosphere 67:S48-S53.
  • Dambacher, J.M., J.W Young, R.J. Olson, V. Allain, F. Galván-Magaña, M.J. Lansdell, N. Bocanegra-Castillo, V. Alatorre- Ramírez, S.P. Cooper and L.M. Duffy. 2010. Analyzing pelagic food webs leading to top predators in the Pacific Ocean: a graph-theoretic approach. Progress in oceanography.doi.org/10.1016/j.pocean.2010.04.011 
  • Ellis, J. K. and J. A. Musick. 2007. Ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in lower Chesapeake Bay and Virginia (USA) coastal waters. Environmental Biology of Fishes 80(1):51-67.
  • Erickson, R. J., J. W. Nichols, P. M. Cook and G. T. Ankley. 2008. Bioavailability of chemical contaminants in aquatic systems. Pages 9-54 In: R. T. Di Giulio and D. E. Hinton, editors. The toxicology of fishes. CRC Press.
  • Escobar-Sánchez, O., F. Galván-Magaña and R. Rosíles-Martínez. 2010. Mercury and selenium bioaccumulation in smooth hammerhead shark Sphyrna zygaena Linnaeus from the Mexican Pacific Ocean. Bulletin of Environmental Contamination and Toxicology 84 (4):  488-491.
  • Escobar-Sánchez, O., F. Galván-Magaña and R. Rosíles-Martínez. 2011. Biomagnification of mercury and selenium in blue shark Prionace glauca from the Pacific Ocean off Mexico. Biological Trace Element Research 144:550-559.
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  • Storelli, M. M., R. G. Stuffler and G. O. Marcotrigiano. 2002. Total and methylmercury residues in tuna-fish from the Mediterranean Sea. Food Additives and Contaminants 19:715-720.
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  • Ventura-Lima, J., M. R. Bogo and J. M. Monserrat. 2011. Arsenic toxicity in mammals and aquatic animals: A comparative biochemical approach. Ecotoxicology and Environmental Safety 74:211-218.
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New to IMBER!

New National Contacts

  •  Egypt

Nayrah Shaltout

National Institute of Oceanography and Fisheries (NIOF)
Cairo, Egypt

Nayrah is involved in the IMBER-endorsed MedSEA project.

Research interests: biogeochemical cycle of the Egyptian Mediterranean and Red Seas; impact of ocean acidification on diatoms and bacteria; Application of BFM Models on Egyptian Mediterranean Sea and the impact of climate change on the fate of persistent organic pollutants.

  •  Greece

Constantin Frangoulis

Institute of Oceanography, Hellenic Centre for Marine Research (HCMR)
Heraklion, Crete, Greece

Research interests: biogeochemical cycles (C, N, toxin flux) and plankton ecosystem functioning

  • Ireland

Peter Croot

Earth and Ocean Sciences
National University of Ireland, Galway (NUI Galway), Ireland

Research interests: trace element speciation, redox behaviour, kinetics, distribution in natural waters; photochemistry, and regional oceanography

  •  Morocco

Karim Himli

Département d’océanographie et Aquaculture
Institut National de Recherche Halieutique (INHR)
Casablanca, Morocco


Soukaina Zizah

Laboratoire d’océanographie Biologique
Institut National de Recherche Halieutique (INHR)
Casablanca, Morocco 

Research interests: primary production in upwelling areas, mesozooplankton analysis, interactions between environmental parameters and plankton

ZIZAH Soukaina
  •  Spain

Xosé Anton Alvarez-Salgado

CSIC Instituto de Investigaciones Marinas,
Vigo, Spain

Research interests: ocean biogeochemistry, dissolved organic matter, coastal upwelling, dark ocean

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Reports from IMBER Endorsed Projects

GENUS (Geochemistry and Ecology of the Namibian Upwelling System)

Kay-Christian Emeis, Institute of Coastal Research, University of Hamburg, Hamburg, Germany


Upwelling systems (zones of coastal and open-ocean divergence in wind-driven surface water flow) are ocean areas where the sub-thermocline ocean exhales nutrients and CO2. They are the largest marine source of CO2 to the atmosphere and vary in time (because they are directly affected by first-order atmospheric circulation patterns on seasonal annual, and interannual timescales) and space (because of small-scale interactions of winds with coastal topography). Massive phytoplankton productivity is supported by upwelled nutrients and re-captures some or all of the CO2 exhaled by upwelling plumes, either directly over the upwelling shelf, or in the adjacent open ocean, when upwelling filaments are injected into the nutrient-poor surface layer. Very high phytoplankton productivity is the basis for spectacularly rich upwelling ecosystems with short trophic paths. All coastal upwelling systems are economically relevant: They comprise less than 1% of ocean´s surface, but support 5% of global marine primary production, and provide 17% of global fish catches (Pauly and Christensen, 1995). Empirical and theoretical evidence showed that these areas have responded to past climate change and are expected to respond to future climate change, since they are uniquely sensitive to global, regional and local changes in atmospheric circulation patterns. They are also dynamically linked to large oceanic pools of old intermediate waters, and coastal upwelling is invariably linked to low oxygen conditions on the shelf. Several coastal upwelling systems have experienced dramatic shifts in ecosystem structure and fish catches (so-called ecosystem regime shifts) in the observed past. Current thinking is that these shifts in ecosystem structure were not exclusively caused by human intervention, but may have been expressions of global or regional shifts in physical drivers. This view is supported by evidence of similarly radical regime shifts that occurred in the geological past. Most projections on consequences of impending or ongoing climate change for coastal upwelling areas postulate an intensification of the physical forcing regime (wind), with more intense, more sustained, or more wide-spread upwelling, although various physical models differ in their reactions to projected climate change.

GENUS II (2013-2015, second phase, funded by the German Federal Ministry of Education and Research) continues to study relationships between climate change, biogeochemical cycles of nutrient elements, radiatively active gases, and ecosystem structure in the coastal upwelling system of the northern Benguela/SE Africa. Phase I of GENUS (March 2009 - April 2012) concentrated on empirical studies (during ship expeditions) of processes of water mass mixing, oxygen and nutrient element supply, food web structure and dynamics in the northern Benguela system over the shelf bordering the Republic of Namibia. These empirical studies were performed during two expeditions with RV Meteor and RV Maria S. Merian (pilot studies) in 2008 and three seagoing expeditions in 2009 (FRV Africana), 2010 (RRS Discovery), and 2011 (RV Maria S. Merian). These expeditions studied rates of ocean circulation, biogeochemical cycling of nutrient elements between water column, biota and sediments, and trophic interactions and energy flows in the food web. The results of these empirical studies are currently being introduced into a hierarchy of numerical models from regional climate, ocean circulation, ecosystems, and energy flows. The models are essential tools to quantify feedback of trophic structures on biogeochemical cycles, and to simulate interactions between shelf ecosystem, the adjacent open ocean, and the atmosphere.


Figure 13. Photo of the RV Maria S. Merian


Figure 14. Food web model based on stable N-isotopes

The co-operation of German research institutions with regional authorities and institutions continues to be highly fruitful and mutually beneficial. The overarching scientific themes of GENUS - enumerated below in Table 1 - remain valid in Phase II, as does the general structure of GENUS with dedicated work packages for physical drivers, material fluxes, and production/consumption processes. The successful capacity building programme will continue during GENUS II to support more junior and senior scientists, as well as other staff from Namibia who are interested in carrying out investigations integrated in GENUS II topics. This has been extended to include qualified candidates from Angola and South Africa. During The involvement of Namibian scientists at local institutions during GENUS I was found to be most beneficial. Consequently, as an alternative to scholarships, a very flexible capacity building support scheme has been designed that will enable Namibians to fulfil their local commitments (e.g., at NatMIRC), while at the same time pursuing their PhD ambitions. The GENUS II capacity building programme (CBP) will thus fund full PhD and/or MSc projects in Germany, and will support PhD projects of professionals from the region, by funding participation in research cruises, workshops, individual scientific activities, visits to German research institutions, purchase of computers and other essential instrumentation, as well as external lab work, e.g. isotope analyses.


Table 1. Comparison of work foci in GENUS Phases I and II under the 4 scientific themes

Science highlights from GENUS I

Hydrography / Modelling:

The shelf – ocean exchange is intensified by mesoscale dynamics and upwelling filaments. Their cross shelf transports exceeded the Ekman-Transport by the factor of 2:3. Actions of swell and internal waves (internal tide) modify the large scale sediment distribution on the Namibian shelf and have a large impact on transport of carbon-rich suspended particulate matter towards the deep ocean.

In detail, results from three GENUS ship expeditions conducted between 2009 and 2011 showed that the attenuation of the wind field north of the Kunene region (ca. 17°S) controls the seaward-directed current at the Angola-Benguela Frontal Zone. Here, the coastal zone acts as an “oceanographic valve” for the poleward undercurrent and the intrusion of nutrient rich and oxygen depleted South Atlantic Central Water (SACW) masses. During the austral summer the coastal poleward undercurrent of SACW was detected as far as the southern limit of the northern Benguela region (Lüderitz at 26.5°S) while the Eastern South Atlantic Central Water (ESACW) was still transported northward along the shelf edge at the same time. Consequently, the region between Lüderitz and Kunene represents the mixing zone of both water masses. Mixing processes result in complex currents, mesoscale dynamics and the evolution of filaments. The advection of each water mass significantly controls the oxygen supply on the shelf of the northern Benguela region with SACW leading to suboxic or anoxic water conditions, whereas ESACW increases the oxygen ventilation. Therefore, at the end of the upwelling season, in austral winter, the oxygen rich ESACW is the dominating water mass on the Namibian shelf; at this time the SACW is pushed back to the Kunene region. However, local oxygen consuming events at around 23°S (Walvis Bay) may still lead to low oxygen concentrations in some parts during that time. Contrastingly, in austral summer SACW is transported with the poleward undercurrent southward to ca. 26°S and results in low to oxygen-free conditions on the entire inner shelf. At the shelf edge, however, ESACW is still the dominant water mass and hence the oxygen supply remains sufficient.

Small-scale filaments directed to the open ocean are characterized by lower temperatures and salinity values, as well as distinctly higher primary production rates, and are spatially and vertically distinctly separated from the surrounding oceanic water masses. However, it occurred that the surface water within a filament quickly warmed-up, so that the filaments were masked with respect to satellite remote sensing using SST. Vertical extension of the filaments ranged between 90-100 m.

The ecosystem model ERGOM from the Institute of Baltic Research in Warnemünde, Germany was successfully applied and extended for the Southeast Atlantic. Additional zooplankton groups and the sulphur cycle were implemented. The model results highlighted the role of large scale central water advection and mesoscale dynamics for the formation and temporal evolution of the Oxygen Minimum Zone. The behaviour of zooplankton (vertical migration) has an important impact on the vertical distribution of oxygen in the water column.


This benthic remineralisation of organic matter was examined along the Namibian coast between 30 – 3000 m water depth. Measured and calculated fluxes show that the efflux of phosphate and ammonium from the sediment was exponentially increasing with increasing temperature, and was generally most intensive at the inner mud belt (100-200 m). Phosphate was also mobilised from sediments with low oxygen concentrations and temperatures above 12°C. High oxygen concentrations restricted the efflux of ammonium by nitrification at high water depths and low temperatures. Denitrification fuelled by water column nitrate was generally found to be limited by the nitrate concentration and was most intensive where nitrate-rich Antarctic Intermediate Water (AAIW) reached the sediment. The production of N2 was mainly a result of coupled nitrification-denitrification processes and correlated well with the total oxygen flux into the sediment. In summary, the water column N:P ratio is markedly decreased by denitrification at oxygen concentrations below 150 µmol l-1. Additional mobilisation of sediment-bound phosphate at oxygen concentrations below 50 µmol l-1 intensifies the apparent N-deficit of the upwelling bottom water.

In the photic zone, nitrogen fixation was expected because of favourable nutrient conditions in the Benguela upwelling area. However, during three research cruises conducted by GENUS between 2009 - 2011, no nitrogen-fixing Trichodesmium spp. were found, nor significant nitrogen fixation measured in this area.

Regarding the carbon cycle, GENUS aimed to study the functioning of the biological pump in the Benguela upwelling system and the adjacent Angolan shelf. Results revealed that CO2 is mostly emitted into the atmosphere on the Angolan shelf, through the decomposition of terrestrial organic matter carried by rivers into the ocean. In the northern Benguela upwelling system, the continental shelf also emits CO2 but acts as a sink for CO2 in the southern part. The opposite functioning of these two upwelling systems reflects the different composition of the subsurface water that wells up along the coast. The subsurface water in the south is much younger than that in the north, which strongly increases the CO2 uptake efficiency of the biological pump on the shelf.


GENUS examined the horizontal and vertical distributions of different groups of meso- and macrozooplankton, their trophic role and their contribution to the oceanic carbon cycle in the high productive Benguela upwelling region. Generally Crustacea made up 80-90% of the individuals, Copepoda Calanoida (50-60%) were numerically the most important organisms in the Namibian upwelling. Overfishing and climate change may lead to an increase in abundance of gelatinous and semi-gelatinous organisms. Cnidaria, Pteropoda, Chaetognatha and Thaliacea were investigated in detail and showed the highest diversity at the shelf break and offshore stations. However, the abundance and mean size of the Cnidaria was higher at the onshore stations, whereas the other groups showed the highest abundance at the shelf break stations. The abundance and composition of zooplankton outside and inside an upwelling filament revealed significant differences between the two water masses with higher concentrations of individuals outside the filament. The fate of the animals that are transported within the filament is still under discussion.

Investigations of calanoid copepods revealed far more complex and sophisticated trophic interactions than previously assumed for coastal upwelling systems. Extensive respiration measurements with a high resolution for copepod species yielded energetic requirements. These data were applied to produce a carbon budget for the Benguela upwelling system and contributed to a food-web model employing the Ecopath with Ecosim (EwE) software package. The EwE model integrates all data on energy requirements and trophic interactions and will help to better understand coastal upwelling systems in terms of ecosystem stability, vulnerability and resilience in the context of environmental change.

Krill occurrence and species composition have been recorded regularly since 2004 between 17 and 23°S. The most important, Euphausia hanseni, was chosen as a pelagic model. Moult (growth) and reproductive strategy were related to the variable environment where effects of upwelling pulses were indicated by synchronisation of growth and reproductive processes. Vertical migration was modified by the seasonal oxygen and trophic regime. Performance of krill species was taken as an indication of foodweb changes.

Regarding ichthyoplankton, GENUS is interested in the consequences of regime shifts on growth, condition, physiology and survival of fish. Fish larvae are the bottleneck in the development of fish populations. Our engagement in the region, including pre-project studies, allows short time series of the abundance and distribution of organisms. A clear increase of horse mackerel larvae and the decrease of sardine in the same period was observed. These trends in larvae distribution and abundance reflect the situation of the fisheries in Namibian waters, showing the increasing importance of horse mackerel in past decades, and the almost complete absence of sardines in the catches. To understand the reasons for this shift the adaption capacity of organisms to environmental changes, especially temperature and oxygen were investigated. Results showed limited reaction of horse mackerel larvae to decreasing oxygen concentrations. Even when decreasing to 10%, the fish recovered within a very short time. We postulate that horse mackerels cope much better with low oxygen than sardines, and thus could take over the niche in the pelagic system.


Figure 15. MOCNESS ready for deployment

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The Atlantic Meridional Transect (AMT) – 22 research cruises between 50°N and 50°S over an 18-year time span

Andy Rees1 (apre@pml.ac.uk) & Mike Zubkov2 (mvz@noc.ac.uk)

1Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, PL1 3DH, UK

2National Oceanography Centre, University of Southampton Waterfront Campus, European Way, Southampton, SO14 3ZH, UK


On 24 November 2012 the 22nd Atlantic Meridional Transect (AMT) cruise arrived  in Punta Arenas, Chile after a voyage of approximately 13,500 km. The AMT is a multidisciplinary programme which undertakes biological, chemical and physical oceanographic research during an annual voyage between the UK and destinations in the South Atlantic – so far, the Falkland Islands, South Africa and Chile. This ocean transect crosses a range of ecosystems from sub-polar to tropical, and from euphotic shelf seas and upwelling systems to oligotrophic mid-ocean gyres. Since 1995, 223 scientists from 18 different countries have been involved in the AMT. The data gathered from the in situ observation system that the project provides for the Atlantic Ocean, between ~50°N and ~50°S, informs on trends and variability in the biodiversity and functioning of the Atlantic ecosystem during in this time of rapid climate and biosphere change .

The AMT observations, in parallel with remote sensing and modelled data, are being interrogated within the EU Green Seas programme (http://www.greenseas.eu/home), to distinguish longer term (decadal) climatology from short-term (inter-annual) variability, in order to assess the ecosystem responses to environmental and climate change.


Figure 16. ChlorophyII-a concerntration determined at the deep chlorophyII maximum during AMT cruises 2 - 20.

AMT is not limited to time series investigations, but also provides an excellent platform for targeted scientific investigation. Ten papers from the AMT were published during 2012 and 2013 on a variety of topics including: the microbial use of methanol, particle backscattering as a function of size structure, and the assimilation of data into a pre-operational physical-biogeochemical model.

Recently a study of the carbonate chemistry of the upper Atlantic Ocean was initiated. Approximately 25% of anthropogenically produced CO2 has been removed from the atmosphere by the oceans and has resulted in a profound change in ocean carbonate chemistry and the resultant phenomenon of ocean acidification. Current evidence indicates that predicted large and rapid changes in ocean pH will have adverse effects on marine calcifying organisms and biogeochemical cycles. AMT provides an excellent opportunity to monitor natural and forced changes in ocean carbon chemistry. To address this, autonomous measurements of surface pCO2 are being enhanced by vertically discrete measurements of pH, DIC and Total Alkalinity.


Figure 17. pH determined spectrophotometrically using  m-cresol-purple dye during AMT-21

One of the underlying tenets of the AMT programme is collaboration and providing opportunities for the international community. Scientists on the RRS James Cook during AMT-22, provided sea-truthing validation of airborne instrumentation deployed by NASA during several over flights of the ship in the vicinity of the Azores. This opportunity was used to improve the functionality and reliability of a research scanning polarimeter, and to increase the capability of an airborne High Spectral Resolution Lidar-1 which has applications for air-sea gas (CO2) exchange, ocean-aerosol interaction and cloud extinction and droplet density.

Colleagues from the UK Met Office and the Laboratoire d'Océanographie de Villefranche in France took advantage to deploy Bio-Argo floats and standard floats in the rarely visited northern and southern hemisphere mid-gyres.

A complete list of AMT publications (currently 220 published articles, including two special issues of Deep-Sea Research II and one of Progress in Oceanography) can be found at: http://www.amt-uk.org/publications.aspx. This unique spatially extensive decadal dataset continues to be expanded and made accessible to the wider community through the British Oceanographic Data Centre (http://www.bodc.ac.uk/projects/uk/amt/). The programme is hosted by Plymouth Marine Laboratory (http://www.pml.ac.uk/) in collaboration with the National Oceanography Centre, Southampton (http://noc.ac.uk/) and provides an exceptional opportunity for nationally- and internationally- driven collaborative endeavours.

Training the next generation of scientists is an integral part of the AMT. So far, more than 60 PhDs have been completed. This has recently been enhanced through the development of the POGO-AMT fellowship programme (http://ocean-partners.org/) to support students and early career researchers from developing nations. Participants are given the opportunity to develop their research skills and collaborate by working closely with experienced researchers.  This will allow them to build their capacity, that could be beneficial for their home institutes and countries. The deadline for the 2013 POGO-AMT fellowship is the 3 May 2013 -see: http://www.ocean-partners.org/training-and-education/research-cruise-training/pogo-amt-fellowships


Figure 18. The AMT has travelled between the UK and South Atlantic since 1995. (AMT cruise tracks, AMT1-11 (yellow), AMT12-17 (red), AMT18-21 (Blue) between 1995 and 2012)


AMT publications 2012-2013:

  • Dixon, J., S. Sargeant, P.D. Nightingale, and J.C. Murrell. 2013. Gradients in microbial methanol uptake: productive coastal upwelling waters to oligotrophic gyres in the Atlantic Ocean. ISME Journal 7: 568-580.
  • Gómez-Pereira, P.R., M. Hartmann, C. Grob, G.A. Tarran, A.P. Martin, B.M. Fuchs, D.J. Scanlan, and M.V. Zubkov. 2013. Comparable light stimulation of organic nutrient uptake by SAR11 and Prochlorococcus in the North Atlantic subtropical gyre. ISME Journal 7: 603-614.
  • Gómez-Pereira, P.R., G. Kennaway, B.M. Fuchs, G.A. Tarran, and M.V. Zubkov. 2013. Flow cytometric identificaiton of Mamiellales clade II in the southern Atlantic Ocean. FEMS Microbiology Ecology 83(3): 664-671.
  • Brewin, R.J.W., G. Dall'Olmo, S. Sathyendranath, and N. J Hardman-Mountford. 2012. Particle backscattering as a function of chlorophyll and phytoplankton size structure in the open-ocean. Optics Express20:17632-17652.
  • Chust, G., X. Irigoien, J. Chave, and R.P. Harris. 2012. Latitudinal phytoplankton distribution and the neutral theory of biodiversity. Global Ecology and Biogeography. doi:10.1111/geb.12016.
  • Dall'Olmo, G., M.J. Behrenfeld, E. Boss, and T.K. Westberry. 2012. Particulate optical scattering coefficients along an Atlantic Meridional Transect. Optics Express 20:21532-21551.
  • Ford, D.A., K.P. Edwards, D. Lea, R.M. Barciela, M.J. Martin, and J. Demaria. 2012. Assimilating GlobColour ocean colour data into a pre-operational physical-biogeochemical model. Ocean Science 8:751-771.
  • Hartmann, M., C. Grob, G.A. Tarran, A.P. Martin, P.H. Burkill, D.J. Scanlan, and M.V. Zubkov. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. Proceedings of the National Academy of Sciences 109 (15):5756-5760.
  • Llewellyn, C.A., D.A. White, V. Martinez-Vicente, G. A. Tarran, and T. J. Smyth. 2012. Distribution of mycosporine-like amino acids along a surface water meridional transect of the Atlantic. Microbial Ecology 64(2), 320-333.
  • Richier, S., A.I. Macey, N. Pratt, Honey, D.C., M. Moore and T.S. Bibby. 2012. Abundances of iron-binding photosynthetic and nitrogen-fixing proteins of Trichodesmium, both in culture and in situ from the North Atlantic. PLoS ONE 7(5), e35571.
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IMBER future events

Call for abstracts for the IMBER Open Science Conference (23-27 June 2014, Bergen, Norway) will be made soon!

The IMBER Open Science Conference - Future Oceans - will be held in Bergen, Norway from 23-27 June 2014

Future Oceans aims to

  • highlight IMBER research results;
  • promote integrated syntheses;
  • develop a plan for the next phase of IMBER science, in the context of the new research initiative - Future Earth

For more information please visit IMBER OSC website

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11th INTECOL Congress - Advancing Ecology and Making it Count.


Part of the centenary celebrations of the British Ecological Society

18-23 August 2013, London


Abstract submission system is open at http://www.intecol2013.org/27_Callforabstracts.html

For more information, go to: http://www.intecol2013.org/index.php

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  • Aberle N., Schulz K. G., Stuhr A., Malzahn A. M., Ludwig A. and Riebesell U. 2013. High tolerance of microzooplanton to ocean acidification in an Arctic coastal plankton community. Biogeoscience 10: 1471-1481. Article
  • Bell J. D., Reid C., Batty M. J., Lehodey P., Rodwell L., Hobday A. J., Johnson J. E. and Demmke A. 2013. Effects of climate change on oceanic fisheries in the tropical Pacific: Implications for economic development and food security. Climatic Change, DOI: 10.1007/s10584-012-0606-2. Article
  • Bignami S., Sponaugle S. and Cowen R. K. (in press). Response to ocean acidification in larvae of a large tropical marine fish, Rachycentron canadum. Global Change Biology. Article
  • Bopp L., Resplandy L., Orr J. C., Doney S. C., Dunne J. P., Gehlen M., Halloran P., Heinze C., Ilyina T., Séférian R., Tjiputra J. and Vichi M. 2013. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences Discussions 10: 3627-3676. Article
  • Brewer P., Kirkwood W. and Gattuso J.-P. 2013. Progress in controlled in situ ocean acidification experiments. Eos, Transactions American Geophysical Union 94(16): 152. Article
  • Doney S.C. and Ducklow H. 2013. Rapid climate change along the West Antarctic Peninsula: impacts from sea-ice to penguins. Flotsam & Jetsam, Massachusetts Marine Educators. (Winter 2013), 42(3): 1 & 15-18. Article
  • Doubleday Z. A., Clarke S. M., Li X., Pecl G. T., Ward T. M., Battaglene S., Frusher S., Gibbs P. J., Hobday A. J., Hutchinson N., Jennings S. M. and Stoklosa R. 2013. Assessing the risk of climate change to aquaculture: a case study from south-east Australia. Aquaculture Environment Interactions 3: 163-175. Article
  • Engel A., Borchard C., Piontek J., Schulz K., Riebesell U. and Bellerby R. 2012. CO2 increases 14C primary production in an Arctic plankton community, Biogeosciences Discussions 9, 10285-10330. Article
  • Hobday A. J. and Evans K. 2013. Detecting climate impacts with oceanic fish and fisheries data. Climatic Change, DOI: 10.1007/s10584-013-0716-5. Article
  • Hobday A.J., Young J.W., Abe O, Costa D.P., Cowen R.K., Evans K., Gasalla M. A., Kloser R., Maury O. and Weng K.C. 2013. Climate impacts and oceanic top predators: moving from impacts to adaptation in oceanic systems. Rev Fish Biol Fisheries. Article
  • Hu L., Avril B., and Zhang J. 2013. Capacity building for sustainable marine research in the Asia-Pacific region. Eos. 94 (2): 21. Article
  • Keul N., Langer G., de Nooijer L. J., Nehrke G., Reichart G. J. and Bijma J. (in press). Incorporation of uranium in benthic foraminiferal calcite reflects seawater carbonate ion concentration. Geochemistry, Geophysics, Geosystems. Article
  • Lan K. W., Evans K. and Lee M. A. 2013. Effects of climate variability on the distribution and fishing conditions of yellowfin tuna (Thunnus albacares) in the western Indian Ocean. Climatic Change, DOI 10.1007/s10584-012-0637-8. Article
  • Lehondey P., Senina I., Calmettes B., Hampton J. and Nicol S. J. 2012. Modelling the impact of climate change on Pacifc skipjack tuna population and fisheries. Climatic Change, DOI 10.1007/s10584-012-0595-1. Article
  • Leite M.C.F. and Gasalla M.A. 2013. A method for assessing fishers’ ecological knowledge as a practical tool for ecosystem-based fisheries management: Seeking consensus in Southeastern Brazil. Fish. Res., Volume 145: 43–53. Article
  • Leu E., Daase M., Schulz K.G., Stuhr A. and Riebesell U. 2013. Effect of ocean acidification on the fatty acid composition of a natural plankton community. Biogeosciences 10, 1143-1153. Article
  • Martin S., Cohu S., Vignot C., Zimmerman G. and Gattuso J.-P. (in press). One-year experiment on the physiological response of the Mediterranean crustose coralline alga, Lithophyllum cabiochae, to elevated pCO2 and temperature. Ecology and Evolution. Article
  • Piontek J., Borchard C., Sperling M., Schulz K. G., Riebesell U. and Engel A. 2013. Response of bacterioplankton activity in an Arctic fjord system to elevated pCO2: results from a mesocosm perturbation study. Biogeosciences 10: 297-314. Article
  • Resplandy L., Bopp L., Orr J. C. and Dunne J. P. (in press). Role of mode and intermediate waters in future ocean acidification: analysis of CMIP5 models. Geophysical Research Letters. Article
  • Roy A.-S., Gibbons S. M., Schunck H., Owens S., Caporaso J. G., Sperling M., Nissimov J. I., Romac S., Bittner L., Mühling M., Riebesell U., LaRoche J. and Gilbert J. A. 2013. Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms. Biogeosciences 10: 555-566. Article
  • Salinger M. J., Bell J. D., Evans K., Hobday A. J., Allain V., Brander K., Dexter P., Harrison D. E., Hollowed A. B., Lee B. and Stefanski R. 2013. Climate and oceanic fisheries: recent observations and projections, and future needs. Climatic Change, DOI 10. 1007/s10584-012-0652-9. Article
  • Salinger M. J. and Hobday A. J. 2013. Safeguarding the future of oceanic fisheries under climate change depends on timely preparation. Climatic Change, DOI 10.1007/s10584-012-0609-z. Article
  • Wang Z.A., Wanninkhof R., Cai W.-J., Byrne R. H., Hu X., Peng T.-H. and Huang W.-J., 2013. The marine inorganic carbon system along the Gulf of Mexico and Atlantic coasts of the United States: insights from a transregional coastal carbon study. Limnology & Oceanography 58(1): 325-342. Article
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Meeting Calendar



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Should you wish to contribute an article for the IMBER Update, please contact Lisa Maddison


Compiled by the IMBER IPO and RPO staff

ISSN 1951-610X