Ecology and conservation of socially learned foraging tactics in odontocetes

Abstract

Culture-group-typical behaviour shared by community members that rely on socially learned and transmitted information-can drive animal adaptations to local environments and thus has the potential of generating specialized behavioural tactics to solve fundamental life challenges, including capturing prey. However, as human activities rapidly change the world in unprecedented ways, animal foraging cultures may no longer represent optimal solutions to local environments. Odontocetes (toothed whales, dolphins and porpoises) are of particular concern because they rely on learned, specialized foraging tactics in habitats highly affected by human activities. We present a global inventory of odontocete foraging tactics to evaluate their cultural underpinnings, vulnerability to human-induced threats and how this knowledge can inform safeguards. Our synthesis reveals a diverse repertoire-190 cases of 36 foraging tactics in 21 species-but highlights that linkages between culture and anthropogenic impacts are generally obscured by a dearth of data on individual identity, social associations and behavioural diffusion. By identifying global patterns, knowledge gaps and common threats to specialized foraging, our review can guide long-term research towards understanding their ecological and evolutionary drivers. This crucial first step towards designing policies that mitigate human impacts on marine habitats may ultimately protect the diverse odontocete behavioural repertoires that contribute to their survival.This article is part of the theme issue 'Animal culture: conservation in a changing world'.

Keywords: animal culture; anthropogenic impact; foraging specialization; odontocete; social learning.

Figure 1.

Ecological and behavioural drivers of foraging tactics in odontocetes. (A) A conceptual framework illustrating the interconnected, fundamental elements—environment, prey and predators—that make up a foraging tactic. (i) Predator–prey interactions are shaped by features of the physical environment, which influence the abundance, movement and behaviour of both (ii) predators and prey. Additionally, (iii) predators’ learning and other transmission processes (e.g. genetic, epigenetic) can further refine these interactions into specialized foraging tactics exhibited by a subset of the population. (B) The framework extends to odontocetes exposed to human activities; such activities can either hinder or promote specialized foraging tactics. Anthropogenic impacts may occur (iv) directly or indirectly—through alterations in (v) the physical environment, (vi) prey abundance or (vii) odontocete behaviour, which can generate (viii) feedback on the effects of human activities, further promoting (blue +) or hindering (red –) the development of specialized foraging. The three exemplar cases show the (C) absent, (D) negative and (E) positive influence of human activities on odontocete foraging tactics. (C) Cooperative wave-washing specialized foraging tactic exhibited by killer whales (Orcinus orca, ecotype B) in the Antarctic Peninsula where groups of killer whales swim in a highly coordinated way to create waves that dislodge Weddell seals (Leptonychotes weddellii) from ice floes [15], in the absence of humans. (D) Fish removal from demersal longlines by sperm whales (Physeter macrocephalus) spread through the Gulf of Alaska after the expansion of longline fisheries increased opportunities for sperm whales to prey on captured sablefish (Anoplopoma fimbria), causing catch and gear loss to humans and increased injury risk to whales [16]. (E) Cooperative foraging between bottlenose dolphins (Tursiops truncatus gephyreus) and artisanal net-casting fishers targeting migratory mullet (Mugil liza) in southern Brazil, where dolphins herd schools towards fishers in shallow estuarine waters and cue when and where fishers should cast nets in a synchronous tactic that benefits both species [14]. Original art by G.F.F. and D.S.M. Please see colour version of figure online.

Figure 2.

The global scope of odontocete foraging tactics. (A) Spatial distribution of 190 documented foraging tactics across 21 species, primarily in the Global North, categorized into 10 broad categories (warm colours: natural foraging tactics; cool colours: human-induced tactics). Putative cultural foraging tactics—those linked to individual identity and supported by evidence of sharing and social learning—are indicated by filled circles. Latitude and longitude were manually jittered for overlapping points and are approximate. Fundamental ecological drivers of foraging tactics for each odontocete species, including (B) whether the tactic primarily relies on the nature of their prey or physical structures (both human-made and natural), as well as the (C) main prey and habitat types (circles proportional to number of tactics, coloured by broad category). (D) The classification of foraging tactics (black) into putative specialized tactics (dark grey) and putative cultural tactics (light grey), based on (i) individual identity information, (ii) evidence of sharing among multiple individuals, (iii) evidence of social learning and (iv) evidence for culture in the form of association between social structure and tactic use and/or diffusion of the tactic through learning; cultural tactics are further evaluated on evidence for discreteness and evolutionary significance (white). (E) Proportion of specialized foraging tactics with known information on the individual identity, sex and/or age of foragers. (F) Proportion of cultural foraging tactics with known information on the social transmission mode. All variables mentioned are fully defined in electronic supplementary material, table S2. Cetacean silhouettes were generated from illustrations provided by Uko Gorter. Please see color version of figure online.

Figure 3.

Threats to and safeguards of odontocetes’ putative cultural traits. Socially learned, specialized foraging tactics are (A) exposed to, and disproportionately affected by, a range of anthropogenic threats, and are (B) protected, or proposed to be protected, by a range of conservation actions. Threats and actions are numbered per the IUCN–CMP Unified Classifications. The foraging tactics are organized into 10 broad categories (electronic supplementary material, table S1): (i) aquaculture-associated foraging, (ii) fisheries interaction, (iii) prey herding, (iv) human-mediated feeding, (v) human–cetacean cooperation, (vi) prey disruption, (vii) shore-based hunting, (viii) prey species specialization, (ix) tool use and (x) seabird interaction. The tripartite network represents the threats to (red inward arrows) and threats that are a consequence of (grey outward arrows) the foraging categories and the existing (green inward arrows) and proposed (purple outward arrows) conservation actions reported in the reviewed studies. Arrows are weighted by the number of tactics within broad categories for which such threats or actions were reported. Original art by D.S.M. and G.F.F. Please see colour version of figure online.