PICTURE an ocean teeming with life: the sky darkened by massive flocks of birds, giant whales clouding the air with the vapour from their blows and as far as the eye can see, schools of fish breaking the surface to escape myriad predators. Such sights were common before we arrived on the scene.
From historical accounts it is clear that today's oceans are a pale shadow of their former glory. We know what happened to the whales - we killed almost all of them - but why aren't the seas swarming with other animals instead? With fewer whales eating them, for instance, you would expect there to be far more krill in the Southern Ocean, but strangely there seems to be a lot less than before. It appears that the oceans have somehow lost their ability to support such an abundance of life.
In recent years, my colleagues and I have begun to suspect the reason for this is that large animals do far more than just gobble up food: they also play a critical role in maintaining and enhancing the productivity of the seas. By removing them, we may have made the oceans a far poorer place.
If these ideas are confirmed, there are profound implications. We would have to completely rethink the way we manage ocean resources. For instance, fishermen have often killed large predators such as seals and whales in the belief that this will increase fish numbers. Our work suggests the opposite is true.
The amount of life the oceans can support ultimately depends on how much food plants make. Photosynthesis can only occur in the sunlit upper layer, and for the microscopic plant cells, or phytoplankton, that do almost all the photosynthesising in the open ocean, there is a huge problem - gravity. A few species float or swim, but most plant cells tend to sink a few metres per day. Not only does this take them away from the sunshine, it also leads to a constant loss of nutrients from the surface layer.
In winter, strong winds churn up the waters, returning some nutrients to the surface. However, in summer, just when there is most light for photosynthesis, surface waters warm, become less dense and stop mixing with the colder water below. The boundary is known as the thermocline, and once particles sink below it, the nutrients they contain are usually lost to the surface ecosystem. As the planet warms, this stratification effect is expected to become stronger, reducing the oceans' productivity.
Limits of growth
The rate at which nutrients are lost is accelerated by the small animals that feed on plant cells. The faeces of animals such as copepods and krill can sink between 100 to 800 metres per day, and fish faeces can sink more than a kilometre per day.
So the growth of phytoplankton and the animals that feed on them effectively converts dissolved carbon and other elements into particles that sink to the sea floor and end up locked away in sediments - a process known as the biological pump. The loss of carbon is not a problem, as carbon dioxide is absorbed from the atmosphere as fast as it is removed from waters, but other elements are in short supply. In large parts of the ocean, for instance, the growth of plants is limited by a lack of iron in the water. Adding soluble iron to the surface waters in these areas creates a bloom of phytoplankton.
What all this means is that the productivity of the oceans depends on the rate at which essential nutrients are delivered to the sunlit layer or are recycled within it.
Until very recently, our understanding of this process was driven largely by studies of physics and chemistry. Winds blowing iron-rich dust from the land, rivers pouring into the sea and the upwelling of deep water were seen as the key processes supplying nutrients to surface waters.
Animals were rarely viewed as players in this process. However, it is now becoming apparent that animals, particularly large ones, play a very important role in delivering and recycling nutrients.
They do so in at least three ways. The first is simply by mixing up ocean waters, which can return some nutrients to the waters above the thermocline (Geophysical Research Letters, vol 37, p L11602). Whenever animals move through the water rather than merely drift with it, some of the water moves along with their bodies - a phenomenon known as "induced drift". Swimming animals also generate turbulence as they cut through the water, redistributing nutrients as they go. This wake turbulence effect may be negligible for small animals, but there is no doubt that dense aggregations of larger animals moving through the thermocline would have a significant local effect.
Every day, vast numbers of marine animals, from microscopic zooplankton to large fish, do move through the thermocline. Most remain in deep water during the day and visit the surface at night. These vertical migrations can involve movements of thousands of metres, and are probably the largest concerted movement of animals on the planet. In addition, air-breathing animals such as whales and seals often dive below the thermocline.
Astonishingly, the movements of animals may be one of the main forces mixing the oceans and redistributing nutrients. According to recent calculations, this force is similar in magnitude to winds and tides (Nature, vol 460, p 624). What's more, these calculations are based on estimates of the current density and abundance of swimming animals. Since animals, particularly larger animals, were far more abundant in the past, their effect would have been much greater.
The second way in which animals can boost ocean productivity is by nutrient scavenging - feeding at depth and bringing nutrients back to the sunlit zone. Sperm whales, for instance, feed on squid and fish at great depths, and defecate at the surface. Models suggest that this recycling of deep material may well be significant for essential elements such as iron.
On a local scale, humpback whales in the Gulf of Maine have also been shown to scavenge nutrients. In fact, they release more nitrogen at the surface than flows in from all the rivers (PLoS One, vol 5, p e13255).
Many other species are known to feed in deep waters on occasion and return to the surface, including seals, penguins, turtles, seabirds and sunfish, so it is possible these animals also return significant amounts of nutrients to surface layers.
Surprisingly, even krill may play a part. While they were thought to live in the upper 200 metres of water, krill have recently been observed at much greater depths. There is footage of krill 3500 metres down on the sea floor, apparently feeding on material that has sunk to the bottom (Current Biology, vol 18, p 282). If krill regularly feed on the sea floor and return to the surface, this may be an important route for bringing nutrients from the sediments back to the surface.
Of course, the opposite process also occurs. Animals that feed near the surface at night and return to deeper waters take nutrients back down with them. We don't yet know on what scale nutrients are removed from and returned to the surface in this way or what the overall net effect is, so the importance of nutrient scavenging to the productivity of the oceans remains to be established.
Recycling nutrients
What is clear is that without species such as sperm whales and humpbacks, surface nutrient levels would be significantly lower in some areas. What's more, by greatly reducing the numbers of air-breathing animals that feed at depth, it is possible that we have unwittingly altered the balance between nutrient return and removal.
The third way in which animals may boost ocean productivity is by recycling nutrients within the sunlit zone. Take the Southern Ocean. It lacks iron because little dust blows off Antarctica, so any mechanism that keeps this element in the surface layer and allows it to be recycled helps to maintain productivity.
The huge populations of krill in these waters are effectively a buoyant reservoir of iron. They incorporate iron into their tissues and, because they are strong swimmers and live for up to seven years, they can keep iron in the upper layer for a long time. A quarter of all the iron in the top 200 metres of water may be found within the bodies of krill.
However, phytoplankton cannot use this iron if it remains locked away in the bodies of krill and sinks to the ocean floor when they die. This where the whales come in.
The idea is that large whales act as fertiliser factories, converting krill into plant food. Whales produce buoyant plumes of faecal material that functions as liquid manure. Recent measurements of the iron content of the faeces of baleen whales by my team show that concentrations in whale faeces are at least 10 million times the background level in seawater (Fish and Fisheries, vol 11, p 203).
Whales probably play only a small role in fertilising the oceans today, but we know from the records of catches by whaling ships that there used to be millions of great whales in the waters around Antarctica in summer. Back then, it is likely that they had a much greater effect. Significantly, there is evidence that when there were more whales, there was also more krill. This may have been the result of a positive feedback cycle. The more whales there were, the more "fertiliser" they would have produced. That would have allowed more phytoplankton to grow, providing more food for krill and thus for whales. As the krill population grew, the total amount of iron stored in these buoyant reservoirs would have increased. And as the whale population grew, the ecosystem would have become ever more productive.
If this picture is correct, the past abundance of life depended on a juggling act that kept lots of iron circulating in the sunlit zone. When we killed the whales, the "balls" fell. As a result, the ocean is no longer able to support the same amount of life.
In other ecosystems, there may be similar mechanisms involving different groups of predators and prey. It is unlikely that the role of animals as buoyant nutrient reservoirs is solely restricted to the Southern Ocean, or exclusively to the iron cycle.
The fertilising role of whales has another implication. Air-breathing predators were thought to be a major "leak" in the biological carbon pump, returning up to a quarter of the carbon captured by phytoplankton to the atmosphere. In fact, whales may actually help remove carbon dioxide from the atmosphere.
Put it all together and the evidence suggests large animals play a big role in the ocean's nutrient cycles. Some changes in marine ecosystems that have been attributed to physical causes may, in fact, be a result of fishing and hunting. According to one recent study, for instance, phytoplankton abundance has declined in eight of the 10 oceanic regions over the past century - especially in areas where many whales and seals have been culled over the past century (Nature, vol 466, p 591).
The idea that large animals affect ecosystem productivity would not surprise terrestrial ecologists. It has long been accepted that large land animals "engineer" the ecosystems on which they depend. When you have seen elephants pushing over trees, it is easy to understand how they can change the landscape. In the sea, it is harder to see how animals can have an effect - especially in an era when whales, seals and large fish are rare as a result of centuries of over-harvesting.
But this does not mean that such effects do not exist; they may just be more subtle and difficult to measure. In fact, ecosystem engineering may actually turn out to be more important in the open ocean than on land because of the cumulative effect of a vast array of organisms acting on all manner of scales simultaneously (Integrative and Comparative Biology, vol 50, p 188).
More whales, more fish
The next step is to quantify the effects animals have through mixing waters, nutrient scavenging and storing and recycling nutrients. Researchers are already working on models of these processes, and we are starting to build up a far better picture of the role animals play, with the help of microelectronic devices that allow us to measure small-scale turbulence and track large animals.
Monitoring the fertilising effect of a pod of whales, although potentially unpleasant to do, could answer questions about the effects of defecation at the surface, such as whether the recycled nutrients are readily available to phytoplankton. If such studies confirm that the overall effect of large animals is to increase marine productivity - or that they did so in the past - it could challenge some long-cherished concepts in marine ecology. For instance, simple models suggest that removing top predators such as seals and whales would increase harvests of intermediate level species such as fish, squid and krill. This has never been taken seriously by fisheries managers, but Japan has used this argument to try to boost support for a resumption of commercial whaling.
None of the models, however, takes account of the recent discoveries about the positive effects of large animals. The intricate feedback loops of marine ecosystems mean the effects of targeting particular species can be counter-intuitive. More realistic models may produce quite different results and support different harvest strategies. It might well be that allowing whales and other large animals to recover to something like their previous levels would boost fish numbers rather than reduce them. That would be great news for the oceans, for conservationists and for fishing communities.
Steve Nicol leads research into Southern Ocean ecosystems at the Australian Antarctic Division, based in Tasmania
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