​​​​​​​​​​​Written in collaboration with Bjarte Bogstad (IMR and chair of ICES Arctic Fisheries Working Group), Harald Gjøsæter (IMR and member of ICES Arctic Fisheries Working Group), Tore Haug (IMR and member of ICES Working Group on Marine Mammal Ecology), and Ulf Lindstrøm​ (IMR and member of ICES Working Group on Integrative, Physical-biological and Ecosystem Modelling). ​

The battlefield

On a global level, the abundance of marine apex predators (marine mammals and large piscivorous fish) has varied substantially over the past five decades. Although the ecological consequences of such predator changes vary among ecosystems, a likely outcome is a cascade effect through the entire food web. The Barents Sea ecosystem (BSE) supports a rich biological diversity, including major fisheries.  However, productivity varies considerably between years and over the past four decades, the BSE has shown shifts in species abundance. Climate change, with increasing temperatures and reduced ice coverage, is one explanation for these changes, and has led to a gradual shift towards more Atlantic species in the past decade. Northeast Arctic cod, harp seals, and common minke whales are the three main top predators that exploit the Barents Sea ecosystem.

Northeast Arctic cod mostly feed in the Barents Sea but spawn upstream along the Norwegian coast. It is a bottom dwelling fish but also frequently uses pelagic habitats to feed on pelagic prey. Harp seals are present in the Barents Sea all year round but are highly migratory. Common minke whales generally migrate into the Barents Sea in early spring and migrate southwards in September/October. Both mammal stocks  have a very flexible foraging behaviour and as a result their diets also vary according to the spatio-temporal variation in prey availability.

In the last decade, the abundance of cod, the most important commercial valuable fish stock in the area, has increased considerably, and is presently at a record high level (ca. 3 million tons at present). In spite of this increase, the growth and condition of cod has remained stable, with only some decrease seen in the size of large, mature cod. During the same period, the abundance of harp seals has declined while the minke whale stock has been at a stable level. However, the body condition (blubber thickness) of these two mammal stocks has decreased. A time series of minke whale blubber measurements from 1992–2013 shows a significant negative trend over the period with particular low values in 2013, but the strongest decline is observed in harp seals.

The lie of the land

How a stock develops over time depends on survival, feeding, and reproduction and the population dynamics are a result of how these factors vary throughout the life cycle and during the year. While food-limitation appears to be the reason behind the changing body condition of both the harp seal and whale populations, the growth and body condition of the cod population has remained relatively unchanged despite a major increase in abundance. Why have cod, harp seals, and minke whales reacted differently?  It appears that cod outperform the sea mammals in the battle for food as there is larger availability of food (mainly capelin) during winter-spring than for marine mammals, as well as a wider range of prey species being available to cod than to marine mammals. Harp seals are more dependent on prey items found close to the ice edge than the other two predator stocks are, which could partly explain why the performance of harp seals is worse than that of the two other main top predators in the area.

Possible mechanisms in predation and competition

Prey in the Barents Sea for the top predators consists of capelin, polar cod,  1-3 year old juvenile herring and blue whiting, deepwater redfish, deepwater shrimp, young specimens  of cod and haddock, many more fish species in the Barents Sea, and macrozooplankton (pelagic amphipods and krill).

Krill abundance in the last decade has been above average and a recent study on harp seals indicates that a high abundance of krill has a positive impact on the seal condition. However, high abundances of capelin, polar cod, and cod and competition between harp seals and cod for shared resources (such as krill) both appear to have a negative impact on the seal condition, which in turn has implications for breeding success. Ice loss further contributes to the decline in harp seal body condition. Less ice means longer migration routes and more energy spent moving between breeding/molting areas and feeding areas along the ice edge. Barents Sea harp seals have faced severe problems with a recent dramatic pup production decrease.

A negative trend in the body condition of minke whales has also been observed over the period 1992–2013, with particular low values in 2013. One factor in this decline is the reduction in the herring stock during the last years, as minke whales overlap considerably with young herring in the Barents Sea.

Competition

The most concentrated overlap of cod and minke distributions is during summer and autumn in the central and northern parts of the Barents Sea where they compete for krill and capelin. Harp seals are also found in open waters from June-October but while there is little spatial overlap between harp seals and the two other predators, food competition still exists. It is not obvious that the food abundance and distribution of predators and prey has changed in a way that would favour cod, in particular medium sized cod, compared to harp seals and minke whales. Perhaps small and medium cod do better because they can utilize low densities of zooplankton which are not attractive for larger predators.

However, one advantage that cod exhibits over harp seals and minke whales is the potential predation space it occupies. When stocks overlap, vertical distribution relative to that of the prey, prey type preferences and ability to catch prey of different species and sizes are the main factors in competition for food.

As a bottom dweller, cod has access to some benthic organisms that are unavailable to seals or whales.  There is a trade-off between energy use and predation for sea mammals because they have to pay an energetic price for diving. Diet studies and diving experiments indicate that minke whales primarily feed in the upper 100 m of the water column. Harp seals use the entire water column but generally only stay submerged for less than 10 minutes, which leaves little time at depth if the animal chose to dive as deep as 300 m.

Migrating north

In recent years, the capelin stock has been of medium or large size. Cod benefits from a large capelin stock while macrozooplankton plays a key role in the diet of the sea mammals. Because capelin directly impacts macrozooplankton abundance through grazing, this may partly explain the negative relationship between seal condition and amount of capelin.

The retraction of the ice edge northwards during the last decade may have opened up new areas for production with ecosystem surveys indicating that macrozooplankton is much more abundant in the marginal northern areas than centrally in the Barents Sea. How might this affect the feeding situations for the predatory stocks?

The lack of zooplankton in central areas of the BSE may be caused by capelin stock moving through this area on the feeding migration northwards. Whether the sea mammals may benefit from increased plankton stocks in the north, depends on whether the capelin halt their northward migration before they reach the northern limit of zooplankton distribution. Minke whales can feed where food is available and may already have found such areas to exploit but because seals are more ice dependent, if the zooplankton rich areas do not extend further north to the ice edge, the harp seals may suffer food shortages more than the whales. The fact that blubber thickness has decreased more among seals than among minke whales indicates that such mechanisms may have been present in recent years.

Looking forward

In the short term, it is expected that cod stocks will decline from the current high level observed and this may result in improved individual growth. Harp seal numbers are also likely to continue to decrease due to recent poor recruitment, but the resulting available per capita food may increase and improve the conditions for the seals.

The Norwegian spring spawning herring stock has suffered from low recruitment for several years, but a strong herring year class may occur any time, which could have a significant negative effect on capelin recruitment. As a result, increased krill biomass, a major component in the diets of both harp seals and minke whales, is therefore likely to be more beneficial to the sea mammals than the cod. ​

In the longer term, increasing water temperatures and a reduction in sea ice may have major effects on the energy flux in the system. Model simulations suggests that reduced sea ice weakens the stratification leading to a higher pelagic production and a lower benthic production which is likely to affect cod more than the mammal predators since cod feed on the benthic community.

Conversely, earlier and prolonged seasonal ice-melt may cause increased disparities between phytoplankton blooms and zooplankton production and as a result lower pelagic production. A recent study suggests that loss of sea ice triggers late autumn phytoplankton blooms. Which predators will benefit most from this is difficult to say, however, changes in the distribution and length of the production period is likely to affect the migration patterns of both cod and the marine mammal. In case of a continued warming, predator and prey stocks are likely to move further north— minke whales will have no problem of feeding successfully in the polar ocean and, to a lesser extent, the same applies for harp seals but cod is not likely to move into deep Polar Ocean.

Deteriorating ice conditions in the White Sea, the main breeding area for Barents Sea harp seals, may force the seals to change to other breeding areas, affecting their migration pattern considerably. Cod migration patterns could also change if new spawning areas such as the Bear Island area or the Novaya Zemlya coast appear. A change of breeding/spawning areas would profoundly change the whole life history of a stock, since this will affect the drift pattern of larvae (fish) and feeding area of the young (seals) in an unpredictable way.

In addition, the gradual shift in species composition towards more Atlantic dominated zooplankton species implies that fatty arctic ice-associated prey such as amphipods is being replaced by less fatty Atlantic species. Less energy-rich food will allow the predators to build up less energy during the feeding season affecting their ability to undertake long migrations to spawning/breeding areas and to develop gonads or suckle their young.

Several dynamics multispecies models have run 'what –if' future scenarios with respect to harp seal, minke whale, cod, capelin, and herring. These scenarios incorporate both direct effects (more whales means less capelin) and indirect effects (more whales means less cod which then means more capelin). Model comparisons are difficult to make with direct effects dominating in some models, indirect in others. Of course, considering ecosystem changes that have been induced by predators is only one way to consider the future possibilities. Less attention has been given to modeling bottom-up effects, but such influences are also important and could be modelled under similar model frameworks. However, multispecies models have so far not incorporated how migration/geographical overlap/spawning areas might change as oceanographic conditions and stock sizes change and so results should be treated cautiously.

The full text of A review of the battle for food in the Barents Sea: Cod vs. marine mammals (Bjarte Bogstad, Harald Gjøsæter, Tore Haug, and Ulf Lindstrøm) published on 25 March 2015 is available in Frontiers in Ecology and Evolution.