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.

Predator‐scale spatial analysis of intra‐patch prey distribution reveals the energetic drivers of rorqual whale super‐group formation

“…At 14 m 3 of water engulfed per lunge (Kahane‐Rapport & Goldbogen, 2018), a humpback whale would have to lunge 48 times per dive (an order of magnitude more than their average) to filter an equivalent volume. These factors, combined with the ability to feed on more manoeuvrable prey enabled by high‐speed, raptorial approaches (Cade et al., 2020), imply that rorqual whales may be energetically required to make active choices regarding what patch and what part of a patch to feed on, further supporting analysis at the informed whale scale.…”

Aerial attack strategies of hawks hunting bats, and the adaptive benefits of swarming

“…In such cases, hunting may actually be more efficient against a denser group of prey. This is true, for example, of large pelagic predators such as baleen whales that exploit the shoaling of their prey during engulfment ( Cade et al 2020 ), and may also be true of raptorial predators that have more opportunities to capture individual prey items when striking at a dense shoal ( Nottestad and Axelsen 1999 ). It is an open question whether and how the confusion effect may operate in other ecological contexts.…”

“…Understanding the detailed behavior of predators is therefore essential to understanding the ecology and evolution of their interactions with prey ( Lima 2002 ; Hein et al 2020 ). For instance, the dynamics of collective motion in schooling fish is not merely influenced by their immediate response to predators ( Magurran and Pitcher 1987 ; Handegard et al 2012 ; Cade et al 2020 ), but is governed by attraction and orientation rules that may themselves have evolved to promote the formation of coherent mobile groups causing cognitive or sensory confusion in predators ( Ioannou et al 2012 ). Likewise, hunting mode has been found to influence the group size dependence of attack frequency and catch success in raptors attacking flocking waders, leading to conflicting selection pressures on group size according to which predator species are present ( Cresswell and Quinn 2010 ).…”

Aerial attack strategies of bat-hunting hawks, and the dilution effect of swarming

“…In such cases, hunting may be more efficient against a denser group. This is true, for example, of those large pelagic predators such as baleen whales that exploit the shoaling of their prey during engulfment (Cade et al 2020), and might also be true of raptorial predators that will have more opportunities to capture individual prey items when striking at a dense school or swam (Nottestad and Axelsen 1999).…”

“…For example, the groupsize dependence of attack frequency and catch success has been found to vary with predator hunting-mode and species in raptors attacking flocks of waders, leading to conflicting selection pressures on group size (Cresswell and Quinn 2010). On a finer scale, the dynamics of collective motion in schooling fish is not only influenced by their direct response to predator behavior (Cade et al 2020;Handegard et al 2012;Magurran and Pitcher 1987), but is also governed by attraction and orientation rules that may have evolved to promote the formation of coherent mobile groups that cause cognitive or sensory confusion in predators . Nevertheless, idealized approaches have long prevailed when modelling predator behavior -from mass action kinetics in models of prey encounter (Hutchinson and Waser 2007), to fixed attack rates in models of prey capture (Morrell and Romey 2008).…”