The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.

Simultaneous high resolution sampling of predator behavior and habitat characteristics is often difficult to achieve despite its importance in understanding the foraging decisions and habitat use of predators. Here we tap into the biosonar system of Blainville's beaked whales, Mesoplodon densirostris, using sound and orientation recording tags to uncover prey-finding cues available to echolocating predators in the deep-sea. Echolocation sounds indicate where whales search and encounter prey, as well as the altitude of whales above the sea-floor and the density of organisms around them, providing a link between foraging activity and the bio-physical environment. Tagged whales (n = 9) hunted exclusively at depth, investing most of their search time either in the lower part of the deep scattering layer (DSL) or near the sea-floor with little diel change. At least 43% (420/974) of recorded prey-capture attempts were performed within the benthic boundary layer despite a wide range of dive depths, and many dives included both meso- and bentho-pelagic foraging. Blainville's beaked whales only initiate searching when already deep in the descent and encounter prey suitable for capture within 2 min of the start of echolocation, suggesting that these whales are accessing prey in reliable vertical strata. Moreover, these prey resources are sufficiently dense to feed the animals in what is effectively four hours of hunting per day enabling a strategy in which long dives to exploit numerous deep-prey with low nutritional value require protracted recovery periods (average 1.5 h) between dives. This apparent searching efficiency maybe aided by inhabiting steep undersea slopes with access to both the DSL and the sea-floor over small spatial scales. Aggregations of prey in these biotopes are located using biosonar-derived landmarks and represent stable and abundant resources for Blainville's beaked whales in the otherwise food-limited deep-ocean.

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...

Communicating animals must balance fitness benefits against the costs of signaling, such as increased predation risk. Cetaceans communicate mainly with sound and near-surface vocalizations can place signalers at risk from shallow-diving E75 E76 MARINE MAMMAL SCIENCE, VOL. 28, NO. 2, 2012 top-predators with acute hearing such as killer whales. Beaked whales are deep divers living in small cohesive groups with little social defense from predation. Little if anything is known about their acoustic communication. Here, eight Blainville's beaked whales were studied with suction cup attached DTags to provide the first report on social communication as a function of diving behavior for any of the 21 ziphiid species. Tagged whales produced two previously unrecorded signals with apparent communicative functions: (1) fast series of ultrasonic frequency modulated clicks (rasps) were recorded from six individuals, and (2) harmonically rich short whistles with a mean fundamental frequency of 12 kHz were recorded from one whale at up to 900 m depth, the deepest whistles recorded from a marine mammal. Blainville's were silent 80% of the time, whenever shallower than 170 m depth and during the prolonged (19 min) silent ascents from vocal dives. This behavior limits the ability of shallow-diving predators to track Blainville's acoustically and may provide a striking example of the evolutionary influence of the risk of predation on animal communication.

Here we use sound and movement recording tags to study how deep-diving Blainville's beaked whales (Mesoplodon densirostris) use echolocation to forage in their natural mesopelagic habitat. These whales ensonify thousands of organisms per dive but select only about 25 prey for capture. They negotiate their cluttered environment by radiating sound in a narrow 20° field of view which they sample with 1.5-3 clicks per metre travelled requiring only some 60 clicks to locate, select and approach each prey. Sampling rates do not appear to be defined by the range to individual targets, but rather by the movement of the predator. Whales sample faster when they encounter patches of prey allowing them to search new water volumes while turning rapidly to stay within a patch. This implies that the Griffin search-approach-capture model of biosonar foraging must be expanded to account for sampling behaviours adapted to the overall prey distribution. Beaked whales can classify prey at more than 15 m range adopting stereotyped motor patterns when approaching some prey. This long detection range relative to swimming speed facilitates a deliberate mode of sensory-motor operation in which prey and capture tactics can be selected to optimize energy returns during long breath-hold dives.