Whales and cephalopods in a deep‐sea arms race

Abstract

Millions of predator–prey interactions between deep-diving toothed whales and cephalopods occur daily in the dark deep sea. While predatory whales developed traits to detect and hunt their prey, cephalopods had to expand their anti-predatory strategies specialized for visual predators, to counteract acoustic predators. Since toothed whale-cephalopod interactions have never been directly observed in the deep sea, it remains unknown what selective pressures and traits evolved from this arms race. Combining current knowledge, we formalize four hypotheses and associated research approaches that will guide future investigation on oceanic predator–prey systems. We identify whale echolocation as an unprecedented armament to hunt distant prey and propose that deep-sea squids avoid acoustic predators by (1) reducing their acoustic cross-section through body shape and posture, (2) deep-sea migration, and (3) not schooling. Toothed whale predation emerges as a potential driver of the cephalopod live-fast-die-young strategy—which may now leave cephalopods at competitive advantage under global change. The pelagic deep sea is an enormous three-dimensional space that poses unique selective pressures. In absence of sun light, the dominant forms of communication are bioluminescence and sound. Diverse, abundant taxa inhabit the pelagic deep sea (water column >200 m). These taxa range from microplankton to meganekton, which may aggregate and migrate, resulting in a dynamic system with patches of high biomass—and rich hunting grounds for oceanic predators. Toothed whales are mammalian top predators that occur in all oceans. Many of these, including beaked and sperm whales, hunt for deep-sea cephalopods, in particular squids (Clarke 2006) (Fig. 1). They have evolved a range of morphological, physiological, and behavioral traits enabling prolonged breath-hold dives to 100 or 1000s of meters (Kooyman 2009). Deep-diving toothed whales (i.e., odontocetes routinely foraging deeper than 200 m) are efficient, often generalist predators, daily capturing hundreds of prey (Visser et al. 2021). Most cephalopods are fast-growing, relatively short-lived predators with a single reproductive cycle followed by death (semelparity), a life history adaptation that is possibly driven by a massive increase in predation pressure subsequent to the evolutionary loss of the external shell (Amodio et al. 2019). Their size and high gonadal investment makes them nutritious prey (Boyle and Rodhouse 2005). The evolution of cephalopod avoidance strategies is strongly rooted in their response to predominantly visual predators. Cephalopods have co-existed with their main predators, fishes, for 530 million years (Jaitly et al. 2022). The much more recent entry of mammals into the marine realm and ensuing evolution of predatory toothed whale echolocation (34 million years ago), created strongly different selective pressures on cephalopod adaptive strategies to avoid predation—this time by acoustic predators. The resulting evolutionary arms race in predator–prey adaptations has shaped the cephalopods and toothed whales into the organisms roaming our modern oceans. Their interactions, however, remain unobserved, and unknown. Have pelagic cephalopods succeeded in eluding large, warm-blooded predators geared for long-range detection of prey? Which traits drive the deep-sea arms race between toothed whales and cephalopods? Here, we combine the current knowledge on deep-diving toothed whale predators and their cephalopod prey (focused on oegopsid squids) to reconstruct their sequence of predatory interactions, from search to selection and capture. In the light of current ecological concepts, we form four testable hypotheses supported by research approaches, advancing to a scientific framework that will help understand the selective pressures shaping deep-sea predator–prey systems. Cephalopods can sense vibrations using a system analogous to the lateral line system of fishes, and rely on