Predator-informed looming stimulus experiments reveal how large filter feeding whales capture highly maneuverable forage fish

Abstract

The unique engulfment filtration strategy of microphagous rorqual whales has evolved relatively recently (<5 Ma) and exploits extreme predator/prey size ratios to overcome the maneuverability advantages of swarms of small prey, such as krill. Forage fish, in contrast, have been engaged in evolutionary arms races with their predators for more than 100 million years and have performance capabilities that suggest they should easily evade whale-sized predators, yet they are regularly hunted by some species of rorqual whales. To explore this phenomenon, we determined, in a laboratory setting, when individual anchovies initiated escape from virtually approaching whales, then used these results along with in situ humpback whale attack data to model how predator speed and engulfment timing affected capture rates. Anchovies were found to respond to approaching visual looming stimuli at expansion rates that give ample chance to escape from a sea lion-sized predator, but humpback whales could capture as much as 30-60% of a school at once because the increase in their apparent (visual) size does not cross their prey's response threshold until after rapid jaw expansion. Humpback whales are, thus, incentivized to delay engulfment until they are very close to a prey school, even if this results in higher hydrodynamic drag. This potential exaptation of a microphagous filter feeding strategy for fish foraging enables humpback whales to achieve 7× the energetic efficiency (per lunge) of krill foraging, allowing for flexible foraging strategies that may underlie their ecological success in fluctuating oceanic conditions.

Keywords: attack kinematics; fish feeding; humpback whale; looming stimulus; predator/prey.

Fig. 1.

This study combined field data, laboratory playbacks, and modeling. Points i–v are time aligned. (A) Suction cup video and 3D accelerometry tags were deployed on anchovy feeding (AF) humpback whales in California, USA. (B) Video recorded the behavior of schools as well as the timing of engulfment in relation to fish schools and to the whale’s own acceleration profile. Fish did not break the school until the mouth opening (MO) event. (C) Mean speed profile of a Type 1 humpback whale. Lunge feeding is most efficient when engulfment coincides with deceleration. (D) Speed and engulfment were parameterized into looming stimuli and played back to anchovies in the laboratory. Anchovies demonstrated C-start escape responses at consistent thresholds of dα/dt. (E) Stimuli parameterized from predator data, as opposed to a constant approach speed, increased rapidly after the tips of the jaws were wider than the whale’s maximum girth.

Fig. 2.

Anchovies are evolutionarily conditioned to avoid small, fast, and mobile particulate feeding predators by forming and reacting as dense schools. Humpback whales, as less commonly encountered predators, take advantage of this strategy in 4 ways: (A) Lunge filter feeding enables engulfment of many individuals simultaneously. (B) MO close to the school results in shorter prey reaction distances equivalent to the whale’s distance at apparent MO (AMO). This value will be intermediate between the 2 extremes of theoretical approaches (mouth always open and mouth always closed). (C) Anchovies at the back of a fleeing school will respond directly to the fish fleeing around it, however, these fish have less time to respond (resulting in a shorter reaction distance) than if they could see the approaching predator directly. (D) Humpback whale flippers can be 3 to 4 m in length—although not themselves used as weapons, they have white undersides that can be used to scare escaping fish back toward the school (see also Fig. 4 and Movie S4).

Fig. 3.

Energy use during lunge feeding is a product of speed and engulfment timing, while catch percentage is a product of kinematics and the timing of engulfment with respect to the school. (A) Energy cost as speed of the mean fast humpback approach is varied. (B) Cost as the timing of MO relative to peak speed of the fast approach is varied. (C) Cost of varying MO timing for a slow approach. (D–F) How catch percentage varies both as a function of school distance at MO and with variation in speed (D) or MO timing (E and F). Thick black lines highlight the mean observed approaches.

Fig. 4.

Efficiency is affected by catch percentage and energy use as shown in Fig. 3. (A) At high speeds, efficiency drops sharply if whales open their mouths too early. Efficiency is increased for moderate speeds when the flippers are used to scare early fleeing fish back toward the mouth. (B) The timing of the MO in relation to the school has a much greater effect on efficiency than the timing in relation to peak speed. (C) At slow speeds, the timing of engulfment is less critical as efficiency can remain high.