Abstract

The largest migration on Earth occurs on a daily basis in the ocean as creatures move up near the surface during the night to feed and descend to the relative safety of the dark depths during the day. This phenomenon is thought to reflect feeding opportunities and predator avoidance according to light levels, but the dynamics of this have rarely been studied. Samuel Urmy and Kelly Benoit-Bird from the Monterey Bay Aquarium Research Institute, USA, inspired by the originally terrestrial concept of ‘landscapes of fear’, sought to investigate if the fear of predation shapes the ecological process of daily migrations.Urmy and Benoit-Bird used an upwards-facing echosounder, which produces sonar pulses and records the returning echoes to detect and visualize schools of fish, squid and plankton, to provide information about their daily vertical movement patterns. Additionally, an underwater microphone next to the echosounder listened for the hunting sounds made by nearby toothed whale predators, such as Risso's dolphins (Grampus griseus) and Pacific white-sided dolphins (Lagenorhynchus obliquidens). Recording the echolocation clicks gave the researchers an indication of the presence of a predator, allowing them to investigate the interactions between the predators and the prey in their vicinity. Successfully collecting data beneath almost 1 km of seawater for more than a year is no easy feat, so the team sent down an unmanned robot to survey the area with video to visually confirm the identities of the different species that they were picking up with the echosounder.Scrutinizing a whole year of deep-sea data, the researchers observed many examples of prey taking evasive action to avoid predators. In one example, a bout of dolphin echolocation clicks triggered a school of fish to cluster together and dive for safety moments later. While such a diving response physically increases the distance between the fish and the predator, the fish's vertical plunge also results in weaker echoes returning from the vulnerable fish, reducing the opportunity for the hunting predator to successfully home in on their fishy prey. In addition, the team could use the distinctive echo signatures produced by different species – such as larger Pacific hake (Merluccius productus) and smaller anchovies (Engraulis mordax) – to provide a best guess for which species were appearing in the echosounder traces when video data were not available. This was especially useful for identifying instances of predation that did not involve an echolocating species, such as an occasion when a school of predatory fish approached a cloud of zooplankton and the tiny creatures dived to avoid the hunters. The scientists also discovered that it sometimes took clusters of zooplankton weeks to return to their usual depth after an encounter with a hungry predator. This shaping of a prey animal's behaviour and movement, even in the absence of a predator, provides evidence that the concept of the ‘ecology of fear’ is indeed applicable in the 3D marine realm and complements recent research on marine ‘soundscapes of fear’, where prey fall silent to avoid detection by predators that could be nearby.The vertical movement of animals in the ocean plays a major part in nutrient recycling, and Urmy and Benoit-Bird demonstrate that the lasting behavioural responses of prey to hunting predators potentially has a major influence on this flow of nutrients. The effect of predators on the behaviour of their prey can thus be more lingering than we had thought. Zooplankton layers in the open ocean are therefore not just governed by forces of nature or their particular lifestyles, but by the ecology of fear too.

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