Tool use is rare in wild animals, but of widespread interest because of its relationship to animal cognition, social learning and culture. Despite such attention, quantifying the costs and benefits of tool use has been difficult, largely because if tool use occurs, all population members typically exhibit the behavior. In Shark Bay, Australia, only a subset of the bottlenose dolphin population uses marine sponges as tools, providing an opportunity to assess both proximate and ultimate costs and benefits and document patterns of transmission. We compared sponge-carrying (sponger) females to non-sponge-carrying (non-sponger) females and show that spongers were more solitary, spent more time in deep water channel habitats, dived for longer durations, and devoted more time to foraging than non-spongers; and, even with these potential proximate costs, calving success of sponger females was not significantly different from non-spongers. We also show a clear female-bias in the ontogeny of sponging. With a solitary lifestyle, specialization, and high foraging demands, spongers used tools more than any non-human animal. We suggest that the ecological, social, and developmental mechanisms involved likely (1) help explain the high intrapopulation variation in female behaviour, (2) indicate tradeoffs (e.g., time allocation) between ecological and social factors and, (3) constrain the spread of this innovation to primarily vertical transmission.

Animal tool use is of inherent interest given its relationship to intelligence, innovation and cultural behaviour. Here we investigate whether shark Bay bottlenose dolphins that use marine sponges as hunting tools (spongers) are culturally distinct from other dolphins in the population based on the criteria that sponging is both socially learned and distinguishes between groups. We use social network analysis to determine social preferences among 36 spongers and 69 non-spongers sampled over a 22-year period while controlling for location, sex and matrilineal relatedness. Homophily (the tendency to associate with similar others) based on tool-using status was evident in every analysis, although maternal kinship, sex and location also contributed to social preference. Female spongers were more cliquish and preferentially associated with other spongers over non-spongers. Like humans who preferentially associate with others who share their subculture, tool-using dolphins prefer others like themselves, strongly suggesting that sponge tool-use is a cultural behaviour.

Few studies of kinship in mammalian societies have been able to consider the complex interactions between home range overlap, association patterns and kinship, which have created a critical gap in our understanding of social evolution. We investigated the association patterns of female bottlenose dolphins, Tursiops aduncus, in the eastern gulf of Shark Bay, Western Australia and found that they depended upon the complex interplay of at least three factors: home range overlap, matrilineal kinship and biparental kinship. While home range overlap was positively correlated with female association patterns, preferred associations were found between females showing as little as 27% home range overlap, and some pairs showed avoidance despite 100% home range overlap. Furthermore, on average, both casual and preferred associations took place between females that were more closely biparentally related than expected by chance and this pattern varied depending upon whether or not pairs of females shared the same matriline.

Tool-use research has focused primarily on land-based animals, with less consideration given to aquatic animals and the environmental challenges and conditions they face. Here, we review aquatic tool use and examine the contributing ecological, physiological, cognitive and social factors. Tool use among aquatic animals is rare but taxonomically diverse, occurring in fish, cephalopods, mammals, crabs, urchins and possibly gastropods. While additional research is required, the scarcity of tool use can likely be attributable to the characteristics of aquatic habitats, which are generally not conducive to tool use. Nonetheless, studying tool use by aquatic animals provides insights into the conditions that promote and inhibit tool-use behaviour across biomes. Like land-based tool users, aquatic animals tend to find tools on the substrate and use tools during foraging. However, unlike on land, tool users in water often use other animals (and their products) and water itself as a tool. Among sea otters and dolphins, the two aquatic tool users studied in greatest detail, some individuals specialize in tool use, which is vertically socially transmitted possibly because of their long dependency periods. In all, the contrasts between aquatic- and land-based tool users enlighten our understanding of the adaptive value of tool-use behaviour.

Dolphins are well known for their exquisite echolocation abilities, which enable them to detect and discriminate prey species and even locate buried prey. While these skills are widely used during foraging, some dolphins use tools to locate and extract prey. In the only known case of tool use in free-ranging cetaceans, a subset of bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia habitually employs marine basket sponge tools to locate and ferret prey from the seafloor. While it is clear that sponges protect dolphins' rostra while searching for prey, it is still not known why dolphins probe the substrate at all instead of merely echolocating for buried prey as documented at other sites. By ‘sponge foraging’ ourselves, we show that these dolphins target prey that both lack swimbladders and burrow in a rubble-littered substrate. Delphinid echolocation and vision are critical for hunting but less effective on such prey. Consequently, if dolphins are to access this burrowing, swimbladderless prey, they must probe the seafloor and in turn benefit from using protective sponges. We suggest that these tools have allowed sponge foraging dolphins to exploit an empty niche inaccessible to their non-tool-using counterparts. Our study identifies the underlying ecological basis of dolphin tool use and strengthens our understanding of the conditions that favor tool use and innovation in the wild.