a1 Australian Antarctic Division, Department of the Environment and Heritage, Channel Highway, Kingston, TAS 7050, Australia
a2 BioSciences Division, British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
A recent review by Ainley et al. has suggested that recent investigations of the ecological structure and processes of the Southern Ocean have “almost exclusively taken a bottom-up, forcing-by-physical-processes approach relating individual species' population trends to climate change”. We examine this suggestion and conclude that, in fact, there has been considerable research effort into ecosystem interactions over the last 25 years, particularly through research associated with management of the living resources of the Southern Ocean. Future Southern Ocean research will make progress only when integrated studies are planned around well structured hypotheses that incorporate both the physical and biological drivers of ecosystem processes.
(Received January 09 2007)
(Accepted March 26 2007)
(Online publication July 13 2007)
p1 current address BirdLife International Global Seabird Programme, Welbrook Court, Girton Road, Cambridge CB3 0NA, UK
In a recent review article, “Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem?”, Ainley et al. (2007) 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:
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. 1995), the US AMLR Program (Hewitt et al. 2003), 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 1997). 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. (2007) 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 2006). 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. 2005) and CCAMLR has organized large-scale surveys of the Southern Indian and South Atlantic (Nicol et al. 2000, Watkins et al. 2004) 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. 2006) 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.
The “krill surplus” hypothesis did not fall out of favour as Ainley et al. (2007) 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 1964, Laws 1977, Croxall et al. 1988, Murphy 1995). 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. 1981) and fur seals (Payne 1977), largely non-existent. Recently, however, both in modelling and empirical terms, reinterpretation and reassessment of these historical events has been undertaken (Mori & Butterworth 2006, Ballance et al. 2006), and there is now a strong research focus on developing models that include food web effects (Hill et al. 2006, Murphy et al. 2007).
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 2005). 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. 2007).
The concept of fishing down the food web was accepted in CCAMLR long before Pauly et al. (1998) 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 2000). 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.
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. 1992, Trathan et al. 1996, Jenouvrier et al. 2005, Massom et al. 2006) and significant correlations have been established between krill recruitment and abundance, and sea ice extent (Loeb et al. 1997). Retreating sea ice has been shown to have an effect on the development of spring blooms (Smetacek & Nicol 2005). Salps are far less common in areas with larger extents of winter sea ice (Nicol et al. 2000, Atkinson et al. 2004). 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. 1995, De La Mare 1997, 2001, Curran et al. 2003) 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. 2006, 2007, Forcada et al. 2005, 2006, Leaper et al. 2006). These relationships are all likely to be mediated through changes in the food web, principally through krill (Murphy et al. 2007). 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. 1988, 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 2005) 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 2006).
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. 2006). 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. 2003). The relationship between krill and MSA has been put forward as a hypothesis (Kawaguchi et al. 2005) 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 2004). 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. 2004), 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. 2006). 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. 2006, Murphy et al. 2007, Trathan et al. 2007). 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. (2007) 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: