A paradigm shift?

In a recent review article, “Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem?”, Ainley et al. (Reference Ainley, Ballard, Ackley, Blight, Eastman, Emslie, Lescroel, Olmastroni, Townsend, Tynan, Wilson and Woehler2007) suggested that Southern Ocean and Antarctic ecological research has been dominated recently by an almost exclusive focus on the physical (and chemical) determinants of ecosystem structure, function and dynamics at the expense of studies of species interactions. Their arguments imply that this amounts to a significant paradigm shift and that:

1. a) the role of higher order predators in structuring marine ecosystems is currently under-appreciated and, particularly, the potential ecosystem effects of the historical removal of great whales and seals (the “krill surplus hypothesis”) is no longer deemed important,

2. b) the ecosystem effects of recent and current commercial fishing is being ignored,

3. c) climate-related explanations of species dynamics and trends are disproportionately favoured.

There is no doubt that there has been a considerable heightening of interest by the climate community in the Southern Ocean over the last two decades and this has led to an explosion in the literature on the oceanography and climatology of the region. This focus is unsurprising given that parts of the Southern Ocean are showing some of the most rapid regional warming anywhere on the planet (Vaughan et al. Reference Vaughan, Marshall, Connolley, Parkinson, Mulvaney, Hodgson, King, Pudsey and Turner2003). However, in many ways this research interest has aided rather than impeded understanding of Southern Ocean ecosystems because it has brought a wealth of interdisciplinary talent to bear on an area about which very little was known 30 years ago. Although many climate and biogeochemical studies have tended to ignore the upper trophic levels, to suggest that there has been no emphasis on species interactions is to ignore the many publications on ecosystem research arising from numerous national and international science programmes.

Long-term systematic data collection under national programmes in the Antarctic have been established to address spatial and temporal data gaps in Antarctic ecology. These programs include: the US Long-Term Ecological Research Program (LTER) (Smith et al. Reference Smith, Baker, Fraser, Hofmann, Karl, Klinck, Quetin, Prézelin, Ross, Trivelpiece and Vernet1995), the US AMLR Program (Hewitt et al. Reference Hewitt, Demer and Emery2003), the UK BAS Programme studies at South Georgia (Murphy et al. 1998), and sub-Antarctic studies at Kerguelen, Crozet and Macquarie islands. Some of these studies have also contributed to international programmes such as the Convention for the Conservation of Antarctic Marine Living Resources (CCAMLR) Ecosystem Monitoring Program (CEMP) (Agnew Reference Agnew1997). Many of the datasets generated by these studies are now approaching 20 years in duration and are hence becoming increasingly valuable in ecosystem analysis. Similarly, the International Whaling Commission (IWC) has over 30 years of data concerning the abundance and trends of populations of Southern Ocean whales, in particular the Antarctic minke whale, through decadal scale, circumpolar sightings surveys. These data have also been subject to substantial analysis, but agreed estimates of population size, trend and structure remain elusive, due particularly to confounding methodological constraints. Thus, national and international effort has been focused on key ecological issues, but many of these datasets are still too short in duration to reliably answer the questions Ainley et al. (Reference Ainley, Ballard, Ackley, Blight, Eastman, Emslie, Lescroel, Olmastroni, Townsend, Tynan, Wilson and Woehler2007) pose.

Individual datasets on particular species at fixed locations do exist and in some cases these have been collected systematically for a longer period (e.g. Croxall Reference Croxall, Boyd, Wanless and Camphuysen2006). There remains, however, a major gap in synoptic data on the distribution and abundance of most species from krill, through seabirds, seals and whales. To help address this SCAR initiated the Antarctic Pack Ice Seals Program in the 1990s to provide information on distribution and abundance of crabeater seals (Southwell et al. Reference Southwell, Kerry and Ensor2005) and CCAMLR has organized large-scale surveys of the Southern Indian and South Atlantic (Nicol et al. Reference Nicol, Pauly, Bindoff, Wright, Thiele, Hosie, Strutton and Woehler2000, Watkins et al. Reference Watkins, Hewitt, Naganobu and Sushin2004) to obtain synoptic data on krill as well as on their predators, lower trophic levels and the physical environment. CCAMLR has also been developing plans to reassess populations of land-based krill predators, particularly those breeding in the south-west Atlantic, in order to address issues relating to the global consumption of krill. The IWC is resolving issues of survey methodology by conducting experimental cruises. Despite all these research efforts, current global estimates of abundance (and hence change in abundance) of most species of Antarctic animals remain highly uncertain. In contrast, our ability to obtain high quality synoptic data on many physical variables, such as sea ice extent and concentration, sea surface temperature and sea surface height, as well as information on ocean colour has greatly increased, so it is not surprising that these broad-scale data have been used to examine ecological relationships. Integrating these data (via ecosystem models) with processes at higher trophic levels requires better data on the distribution and abundance of the key animal species.

Encouragement to give more attention to the role of upper trophic level consumers in the functioning of marine systems is a welcome message. Indeed, some of us contributed Southern Ocean perspectives to a recent volume (Boyd et al. Reference Boyd, Wanless and Camphuysen2006) entitled “Top Predators and Marine Systems: their Role in Monitoring and Management” The theme of this book is the need to understand the complex interactions between biological and physical attributes of the environment, which drive the bottom-up and top-down processes by which marine ecosystems are regulated and organized, if we are to manage commercial fisheries (and other anthropogenic impacts) without detriment to natural consumers and other key components of these ecosystems.

Food chain effects & the “krill surplus”

The “krill surplus” hypothesis did not fall out of favour as Ainley et al. (Reference Ainley, Ballard, Ackley, Blight, Eastman, Emslie, Lescroel, Olmastroni, Townsend, Tynan, Wilson and Woehler2007) suggest. It is just difficult to support or refute without appropriate long-term, systematically collected, datasets on krill and its major predators. With a few notable exceptions, we are not in a position to be able to indicate whether most of the major krill consumers have globally increased or decreased as a result of the demise of the great whales, nor how these predators might now be responding to the recovery of some of these whale populations. Furthermore, we remain unable to estimate robustly global krill consumption now or in the past; data which are essential for examining the krill surplus hypothesis.

We believe that there have been exceptional levels of interest in ecosystem interactions involving top predators in the Southern Ocean. In particular the appreciation of the effects of fishing down the food chain, including the reallocation elsewhere of krill formerly consumed by other top predators (e.g. whales, seals), was widely appreciated and depicted (e.g. Sladen Reference Sladen, Carrick, Holdgate and Prevost1964, Laws Reference Laws and Llano1977, Croxall et al. Reference Croxall, McCann, Prince, Rothery and Sahrhage1988, Murphy Reference Murphy1995). However, the data to assess the likely nature and magnitude of the reconfigurations of energy flow in upper trophic levels, let alone their effects on population trends, were, except for some compelling but circumstantial data for penguins (e.g. Croxall et al. Reference Croxall, Rootes and Price1981) and fur seals (Payne Reference Payne1977), largely non-existent. Recently, however, both in modelling and empirical terms, reinterpretation and reassessment of these historical events has been undertaken (Mori & Butterworth Reference Mori and Butterworth2006, Ballance et al. Reference Ballance, Pitman, Hewitt, Siniff, Trivelpiece, Clapham, Brownell, Estes, DeMaster, Doak, Williams and Brownell2006), and there is now a strong research focus on developing models that include food web effects (Hill et al. Reference Hill, Murphy, Reid, Trathan and Constable2006, Murphy et al. Reference Murphy, Watkins, Trathan, Reid, Meredith, Thorpe, Johnston, Clarke, Tarling, Collins, Forcada, Shreeve, Atkinson, Korb, Whitehouse, Ward, Rodhouse, Enderlein, Hirst, Martin, Hill, Staniland, Pond, Briggs, Cunningham and Fleming2007).

Impacts of recent finfish harvesting

The records of significant fishery catches in the Southern Ocean indicate that commercial levels of fish were first taken in the early 1970s - a full decade later than is suggested by Ainley et al. - so it is unlikely that the commencement of Southern Ocean commercial fishing played a part in the changes in vertebrate populations observed in the Antarctic and sub-Antarctic. Despite the failure of the stocks of Antarctic cod Notothenia rossi Richardson in the Antarctic Peninsula sector (and, to a lesser extent, mackerel icefish Champsocephalus gunnari Lönnberg at South Georgia) to recover following over-harvesting, it is unwise to regard the localized overexploitation of certain finfish species as having remotely comparable effects on the ecosystem to the removal of seals and whales.

The removal of fish from the Southern Ocean ecosystem was locally significant but under no circumstances could it be described as “massive”. Reported removals of fish from the Southern Ocean total some 3 million tonnes over a 36 year period (CCAMLR data). This is relatively modest compared to other world fisheries, some of which exceed this level of catch in a single year. Contrast these catches to the reported landings of krill over the same period (6.6 million tonnes) or the removal of 1.5 million great whales and similar numbers of fur seals and elephant seals, and it is obvious that there may have been localized ecosystem effects as a result of finfish fisheries but there are unlikely to have been direct global-scale effects - other than as a result of seabird bycatch.

Although fish are “the most important predators in most marine ecosystems” this is unlikely to be the case in the Southern Ocean, now or in the past. This may be because the Southern Ocean is dominated by populations of air-breathing vertebrates which may have been removed historically in other parts of the globe or because the structure of the krill-based ecosystem is somewhat different from its northern counterparts (Smetacek & Nicol Reference Smetacek and Nicol2005). There is however, no doubt, that fish are important in Southern Ocean food webs, and the recognition of their role as alternative prey species to krill in some areas has highlighted the need to improve quantification of their current status and trophic interactions (Murphy et al. Reference Murphy, Watkins, Trathan, Reid, Meredith, Thorpe, Johnston, Clarke, Tarling, Collins, Forcada, Shreeve, Atkinson, Korb, Whitehouse, Ward, Rodhouse, Enderlein, Hirst, Martin, Hill, Staniland, Pond, Briggs, Cunningham and Fleming2007).

The concept of fishing down the food web was accepted in CCAMLR long before Pauly et al. (Reference Pauly, Christiansen, Dalsgaard, Froeser and Torres1998) suggested it; indeed, it was the fundamental concern that underlay the ecosystem approach that CCAMLR adopted. It is likely that there have never been large stocks of fish in the Southern Ocean, particularly stocks of small pelagic species which have, some suggest, been replaced by krill (Hamner & Hamner Reference Hamner and Hamner2000). Thus, once the great whales and seals were over-exploited, and localized fish stocks were depleted there remained only one large exploitable stock in the Southern Ocean - krill. Significantly, it was the obvious abundance of krill and its ease of harvesting, rather than the depletion of local fish stocks that led to experimental harvesting in the 1960s and 1970s. The lack of diversity of species with commercial potential in the Southern Ocean contrasts sharply with other oceans where large tonnages of a wide variety of demersal and commercial fish species have been simultaneously harvested for centuries.

Bottom-up and top-down controls on ecosystem processes

Self-evidently, both bottom-up and top-down processes, and other interactions (to varying extents both temporally and spatially) govern ecosystem responses, including anthropogenic influence and this applies particularly to the krill-based ecosystem. Evidence for a physical causation behind some observed ecological changes is well established. Sea ice is known to affect the breeding success of both emperor and Adélie penguins (Fraser et al. Reference Fraser, Trivelpiece, Ainley and Trivelpiece1992, Trathan et al. Reference Trathan, Croxall and Murphy1996, Jenouvrier et al. Reference Jenouvrier, Barbraud and Weimerskirch2005, Massom et al. Reference Massom, Stammerjohn, Smith, Pook, Iannuzzi, Adams, Martinson, Vernet, Fraser, Quetin, Ross, Massom and Krouse2006) and significant correlations have been established between krill recruitment and abundance, and sea ice extent (Loeb et al. Reference Loeb, Siegel, Holm-Hansen, Hewitt, Fraser, Trivelpiece and Trivelpiece1997). Retreating sea ice has been shown to have an effect on the development of spring blooms (Smetacek & Nicol Reference Smetacek and Nicol2005). Salps are far less common in areas with larger extents of winter sea ice (Nicol et al. Reference Nicol, Pauly, Bindoff, Wright, Thiele, Hosie, Strutton and Woehler2000, Atkinson et al. Reference Atkinson, Siegel, Pakhomov and Rothery2004). The exact mechanisms and processes that underlie these relationships are not always well known but there is little doubt that sea ice is a major ecological forcing factor in the Southern Ocean and measurements of current changes in regional and global distributions of sea ice are readily available. Past changes in sea ice distribution are more difficult to measure and attempts to examine pre-satellite trends have required a degree of ingenuity and the use of proxies. The concept of a significant decline in sea ice in the 1950s–1970s is not as widely discounted as has been suggested (Murphy et al. Reference Murphy, Clarke, Symon and Priddle1995, De La Mare Reference De La Mare1997, Reference De La Mare2001, Curran et al. Reference Curran, Van Ommen, Morgan, Phillips and Palmer2003) and if such a major physical change did occur in the Southern Ocean, there is every reason to suspect that it would have had profound ecological consequences. Correlations have also been reported between ocean temperatures and the breeding success of various other species of upper-trophic level predators (Trathan et al. Reference Trathan, Murphy, Forcada, Croxall, Reid, Thorpe, Boyd, Wanless and Camphuysen2006, Reference Trathan, Forcada and Murphy2007, Forcada et al. Reference Forcada, Trathan, Reid and Murphy2005, Reference Forcada, Trathan, Reid, Murphy and Croxall2006, Leaper et al. Reference Leaper, Cooke, Trathan, Reid, Rowntree and Payne2006). These relationships are all likely to be mediated through changes in the food web, principally through krill (Murphy et al. Reference Murphy, Watkins, Trathan, Reid, Meredith, Thorpe, Johnston, Clarke, Tarling, Collins, Forcada, Shreeve, Atkinson, Korb, Whitehouse, Ward, Rodhouse, Enderlein, Hirst, Martin, Hill, Staniland, Pond, Briggs, Cunningham and Fleming2007). The dynamics of the krill-based ecosystem are affected by both top down and bottom up processes, and the balance may well differ temporally and spatially (Murphy et al. Reference Murphy, Morris, Watkins, Priddle and Sahrhage1988, 2007). Many recent reviews have adopted this mixed model perspective either through viewing the animals and plants of the ocean as being active players in the biogeochemical cycle (Smetacek & Nicol Reference Smetacek and Nicol2005) or by interpreting the life cycle of key species as being a complex interaction between the evolved life cycle and their physical, biological and chemical environment (Nicol Reference Nicol2006).

With the Antarctic we are dealing with an entire continent and around this there is considerable habitat and environmental diversity. There are clear physical and biological links between these regions, but processes occurring at the Antarctic Peninsula are sometimes assumed to be equally applicable to the Ross Sea, yet there are major environmental differences between the two regions. There is considerable evidence to indicate that, like other oceans, subdivision into a number of distinct ecological regions both meridionally and latitudinally can be useful (Nicol et al. Reference Nicol, Worby, Strutton, Trull and Robinson2006). Ainley et al. carefully define the ecosystem that they are dealing with - the Antarctic Marine Ecosystem; the pelagic, continental slope ecosystem - yet some of their analysis deals with the Ross Sea or with the sub-Antarctic ecosystems which contain demonstrably different food webs. They also use datasets that have been derived from widely separated sites and which are incompatible. Figure 1 in Ainley et al. compares MSA (methanesulphonic acid) in ice cores taken in East Antarctica to krill from net tows in the South Atlantic and is misleading to say the least. The MSA record has been used to suggest a decrease in the annual extent of sea ice off East Antarctica - an event the authors tend to dismiss - but there has never been any serious attempt to quantitatively correlate MSA and krill and it would be unwise to do so when they are being sampled on different sides of the continent (Curran et al. Reference Curran, Van Ommen, Morgan, Phillips and Palmer2003). The relationship between krill and MSA has been put forward as a hypothesis (Kawaguchi et al. Reference Kawaguchi, Kasamatsu, Watanabe and Nicol2005) but, as is the case with so many other Southern Ocean hypotheses, the data required to test it do not yet exist. Developing integrated analyses of Southern Ocean ecosystems requires an understanding and quantification of both the degree of trophic distinction and separation between sub-systems as well the physical and biological links between systems.

There is no doubt that the removal of great whales, persistent fishing and increases in the abundance of gelatinous organisms may well have had an effect on Southern Ocean ecosystems - but this has happened during a period of unprecedented climatic change (Croxall & Nicol Reference Croxall and Nicol2004). Disentangling causative relationships in a marine ecosystem is fraught with difficulty. What is required, however, is the development of well structured hypotheses that might allow the examination of these factors as well as the physical factors that have been implicated by others. In the absence of suitable long-term data on most of the key animals it will require focussed modelling efforts as well as large-scale field studies to disentangle the processes involved. These approaches are already underway as part of the research efforts of both national and international programmes such as Southern ocean GLOBEC (Hofmann et al. Reference Hofmann, Wiebe, Costa and Torres2004), CCAMLR and the IWC However, other recent initiatives are also focussed on understanding some of the key issues in the Southern Ocean food web.

Over the last four years, recognition of the importance of linking climate related effects and ecological interactions (including control mechanisms in food webs) has led to the development of the Southern Ocean ICED (Integrating Climate and Ecosystem Dynamics) programme (Murphy et al. Reference Murphy, Hofmann and Johnston2006). This programme builds on earlier studies of biogeochemistry and ecosystems (within Southern Ocean GLOBEC and CCAMLR), and specifically considers how ecological and climate related processes interact to affect the dynamics of circumpolar Southern Ocean ecosystems. This is an exciting time in Southern Ocean ecosystem science, especially because long-term (>25 yr) and large-scale (e.g. circumpolar from satellites) datasets are now available allowing integrated studies to be undertaken (e.g. Nicol et al. Reference Nicol, Worby, Strutton, Trull and Robinson2006, Murphy et al. Reference Murphy, Watkins, Trathan, Reid, Meredith, Thorpe, Johnston, Clarke, Tarling, Collins, Forcada, Shreeve, Atkinson, Korb, Whitehouse, Ward, Rodhouse, Enderlein, Hirst, Martin, Hill, Staniland, Pond, Briggs, Cunningham and Fleming2007, Trathan et al. Reference Trathan, Forcada and Murphy2007). There are also studies developing under the Census of Antarctic Marine Life (CAML). With the science developing so rapidly we would encourage Southern Ocean researchers to take an active part in the development of existing circumpolar ecosystem analyses. These should enable us to address the fundamental questions about the major control mechanisms involved in determining the response of Southern Ocean ecosystems to harvesting and climate related perturbations.

In conclusion, we hope that readers may now better appreciate which of the questions posed by Ainley et al. (Reference Ainley, Ballard, Ackley, Blight, Eastman, Emslie, Lescroel, Olmastroni, Townsend, Tynan, Wilson and Woehler2007) are really relevant and some of the current efforts to address these. In essence, there seems little evidence that there has been an “almost complete shift in paradigms”; rather there has been a broadening of the focus of scientific studies. Research priorities in Southern Ocean marine science have indeed seen major shifts in focus, both between biological and physical themes, and between academic and management objectives. Although we believe there has been better integration of the results, especially via CCAMLR, than in most marine systems, this is certainly no cause for complacency. Two challenges face Antarctic marine ecosystem science over the next few years:

1. 1. to ensure that the opportunity of the International Polar Year is used to initiate truly coordinated and interdisciplinary studies (building on studies undertaken over the past 30 years) to develop integrated ecosystem analyses under programmes such as ICED and CAML, and

2. 2. that the results are used by CCAMLR and others to help develop a comprehensive system of environmental management protection for the Southern Ocean to prevent, for the foreseeable future, the overexploitation that characterized it until very recently.

Addressing these challenges will require that marine ecosystem studies utilize the full range of expertise and data available to investigate the entire system from the physical environment to the higher order predators.