Fear of Killer Whales Drives Extreme Synchrony in Deep Diving Beaked Whales

Abstract

fear of predation can induce profound changes in the behaviour and physiology of prey species even if predator encounters are infrequent. for echolocating toothed whales, the use of sound to forage exposes them to detection by eavesdropping predators, but while some species exploit social defences or produce cryptic acoustic signals, deep-diving beaked whales, well known for mass-strandings induced by navy sonar, seem enigmatically defenceless against their main predator, killer whales. Here we test the hypothesis that the stereotyped group diving and vocal behaviour of beaked whales has benefits for abatement of predation risk and thus could have been driven by fear of predation over evolutionary time. Biologging data from 14 Blainville's and 12 Cuvier's beaked whales show that group members have an extreme synchronicity, overlapping vocal foraging time by 98% despite hunting individually, thereby reducing group temporal availability for acoustic detection by killer whales to <25%. Groups also perform a coordinated silent ascent in an unpredictable direction, covering a mean of 1 km horizontal distance from their last vocal position. This tactic sacrifices 35% of foraging time but reduces by an order of magnitude the risk of interception by killer whales. these predator abatement behaviours have likely served beaked whales over millions of years, but may become maladaptive by playing a role in mass strandings induced by man-made predator-like sonar sounds. Deep-diving marine mammals are expected to maximise time spent foraging in deep prey layers to offset the energetic and physiological costs of diving 1. But Cuvier's and Blainville's beaked whales (Ziphius cavirostris and Mesoplodon densirostris, respectively) employ a diving behaviour unlike that of other deep-diving toothed whales: they restrict echolocation to the deepest part of long and deep foraging dives that are typically followed by extended series of shallower and silent non-foraging dives that result in less than 20% of time devoted to biosonar-mediated foraging 2-5. Further, these species ascend slowly and silently from deep dives at a low pitch angle 2. This unusual and costly diving style has been interpreted as serving to mitigate decompression sickness or to accommodate lactate build up from foraging dives that may exceed the aerobic dive limit 6 , but, see 7. However, satisfactory physiological mechanisms to support these interpretations have yet to be found. When other toothed whales dive to similar depths, they do not display such a diving behaviour: both pilot whales that are similar in size to these beaked whales and the larger sperm whales ascend nearly vertically from their deep foraging dives 8,9 and often emit calls during the ascent to mediate reunion with non-diving group members 10-13. Because the highly stereotyped group diving and vocal behaviour of beaked whales is difficult to explain by foraging niche or physiology 2 an alternate proposition is that it serves to abate predation risk 2,4,14. Fear of predation can induce profound...

Deep-diving beaked whales dive together but forage apart

“…Blainville's performed foraging dives that lasted on average 49.4 ± 6.5 min with vocal periods lasting a mean 24.2 ± 5 min, while Cuvier's dives lasted 59.3 ± 10.5 min during which they were vocal 33.9 ± 7 min. The two pairs of whales tagged simultaneously in the same social group demonstrated highly coordinated dives [23] ( figure 1, electronic supplementary material, figure S1). Tags carried by each whale received clicks produced by the other tagged animal of the pair in 100% of the coincident vocal minutes when both tagged whales were clicking (figure 1).…”

“…R. Soc. B 288: 20201905 risk losing the group and the benefits of sociality, such as reduced predation risk [23]. Allaying predation risk may be an especially strong evolutionary driver of the behaviour of Cuvier's (and most probably also Blainville's) beaked whales, given their strong responses to orca sounds and naval sonar [44][45][46].…”

“…Our data suggest that the behavioural tactic employed by beaked whales to reduce intra-group competition for prey is that group members diving in tight coordination spread out when foraging at depth. However, they then reunite to ascend together, avoiding the need to vocalize near the surface where they are more vulnerable to predator attacks [23]. This behaviour might have co-evolved with small group sizes so that individuals can swim close enough to each other to coordinate their movements during dives, but sufficiently apart to find unexploited prey patches.…”

“…In the two instances when pairs of whales were tagged in the same social group, the independence of the click rates of the pair was investigated. These data, previously analysed by Aguilar de Soto et al [23] consisted of highly synchronized dive profiles and vocal periods. The independence of the click rates of the pairs was tested by comparing the time-paired minute average ICI sequences of the two whales with a Pearson correlation test.…”

Hunters versus hunted: New perspectives on the energetic costs of survival at the top of the food chain

“…Far less is known about fear responses of marine mammals although increasing evidence suggests that some mass stranding events by cetaceans may involve a fear response to anthropogenic noise exposure (Aguilar de Soto et al., 2020; Frantzis, 1998; Jepson et al., 2003). As found for terrestrial mammals, predation avoidance strategies in aquatic mammals range from freezing in place to active escape behaviours, but with important differences in physiological function along the oxygen pathway.…”