Sunday, 12 January 2020

Fratercula arctica: Tool use observed in Atlantic Puffins, the first known example of this behaviour in a Seabird.

The evolution of tool use is one of the most enduring puzzles in behavioural biology. Investigating the distribution of tool use across different species is key to understanding its adaptive value and hence its evolution in the natural world, and ultimately to understanding the evolutionary history of our own species. Tool use is the exertion of control over an object with the goal of altering the physical properties of another object, substance, surface or medium, or controlling the flow of information between the tool user and the environment or other organisms in the environment. Tools can be used for several purposes, mainly related to feeding, defence, aggression, social displays, or physical maintenance. True tool use requires manipulation of an object detached from the substrate, unlike borderline tool use where the tool remains part of the substrate. Tool use is a rare but phylogenetically widespread behaviour in the wild. It is most common in Birds and Mammals, mainly in the Passeriformes and Primates, some of which use or even manufacture tools to complete complex tasks. Tool use appears to span a continuum between two broad types: genetically based behavioural specialisations, inflexible and applied in a single context, and more flexible behavioural innovations, whose development may also rely partially on genetics but which can be applied creatively to new contexts. The ability of animals to use tools creatively has been linked to their cognitive capacities. Animal tool use is most frequent, and has been most discussed, in a need-for-resources framework, mainly related to feeding. Using tools for physical maintenance is also relatively common; for example, chimpanzees use tools to groom, scratch, or wipe themselves. In birds, captive Parrots have been reported to scratch with sticks, but to date the only avian tool use for physical maintenance reported in the wild is 'anting', depositing Ants on one’s plumage, which is observed in many species, but mostly Passerines.

In a paper published in the Proceedings of the National Academy of Sciences of the United States of America on 30 December 2019, Annette Fayet of the Department of Zoology at the University of Oxford, Erpur Snær Hansen of the South Iceland Nature Research Centre, and Dora Biro, also of the Department of Zoology at the University of Oxford,provide evidence of a wild Seabird performing another form of tool use for physical maintenance.

Fayet et al. observed two Atlantic Puffins, Fratercula arctica, Charadriiform Seabirds (i.e. members of the group that also includes Sandpipers, Plovers, Gulls, Auks, and their relatives), scratching with a stick. They describe our observations and discuss their implications in the context of animal tool use. 

Puffins nest on colonies around the North Atlantic, mostly on grassy slopes on predator-free islands. As part of a study on Skomer Island, Wales, observations have been made each June since 2012 at dusk, when Puffins gather on the colony to preen, sleep, and socialise. The Birds’ behaviour was observed with a spotting scope. On 18 June 2014 on Skomer Island an adult Puffin was observed holding a wooden stick in its bill and using it to scratch its back for about five seconds. The Bird was sitting on the sea under the colony’s cliffs, among other members of the same species. Shortly thereafter the Bird took off (still holding the stick, albeit it is unclear for how long) and was lost from view.

In July 2018, Browning motion-activated cameras were deployed near Puffin nests on Grimsey Island, Iceland, to record patterns of nest attendance. The cameras were configured to record ten seconds of footage after each movement detection, with a minimum thirty second pause after each video. On 13 July 2018 on Grimsey Island a camera trap recorded similar behaviour. In the video, an adult Puffin picks up a wooden stick from the ground then uses it to scratch its chest feathers. The video stops shortly after this first bout of scratching. On later videos, the stick is on the ground. It eventually disappears after about twenty four hours, presumably displaced by a Bird or the wind.

Puffin scratching with a stick. Grimsey Island, Iceland. Fayet et al. (2019).

The two instances of Puffins using a stick as a tool for body care represent recorded evidence of a wild Bird exhibiting this behaviour, while to date, in the wild only primates and elephants have been observed scratching with a tool. It is also evidence of true tool use in a Seabird, confirming the behaviour in an avian order previously thought to lack the ability, need, or opportunity to use tools. Furthermore, this suggest that while this behaviour is rare it is not restricted to a single population. Each of these conclusions has important implications for our understanding of the distribution and adaptive significance of tool use in the animal kingdom.

Screenshots of a Puffin scratching with a stick. Time stamps (hours: minutes: seconds) indicate time elapsed since the first panel. The stick’s location is indicated by an arrow. (A) Puffin picking up the stick. (B) Puffin holding the stick. (C) Puffin scratching its chest with the stick. (D) Nine hours later, the stick is still visible on the ground. Fayet et al. (2019).

The observations of Puffins rubbing their body with a stick fit the definition of tool use, as they involved the direct manipulation of a detached object toward a specific part of the environment (the Birds’ plumage) with a specific goal. It is important to note that the observations cannot be mistaken for the collection of nest material. Puffins preferentially collect soft material like grass or feathers to line their nests then quickly carry these inside their burrow, as frequently observed on both study colonies. In Wales, the Puffin was sitting on the water and therefore was not collecting nest material on land. Puffins often assemble in rafts near the colony to rest, preen, and bathe. The observed Puffin engaged in body care like many of its neighbours and most likely picked up the stick on land before flying to the water. In Iceland, videos recorded after the tool-use episode showed the stick on the ground, confirming that the Bird did not take it to its nest. Fayet et al. are therefore confident that our observed Puffins did not pick up the sticks as nest lining material.

Puffin taking a feather inside its burrow to line its nest. Grimsey Island, Iceland. Fayet et al. (2019).

Using sticks is common across tool-using taxa, but mostly in a foraging context to extract food from a cavity. Fayet et al.'s observations aside, stick tool use has exclusively been documented for extractive foraging in wild Birds, which remains the primary use even in Primates. Other, less common uses include communication or defence such as Chimpanzee dominance displays, investigation of novel objects by captive New Caledonian Crows, and scratching by Primates, wild Elephants, and captive Parrots. Since the observed Puffins appeared to be rubbing the sticks on their plumage, it is reasonable to rule out foraging, investigation, or communication as the behavior’s function: Puffins only catch prey underwater, and they were not interacting with other Puffins or probing objects with the stick. As such, they were most likely engaged in body care.

Puffin taking grass inside its burrow to line its nest. Grimsey Island, Iceland. Fayet et al. (2019).

Two alternatives for the function of the stick can be proposed: It may have been used for its mechanical properties, to dislodge parasites or relieve an itch, or its chemical properties, in a manner similar to anting, where Birds rub Ants or plants on their plumage, presumably for their antiparasitic properties. The latter hypothesis seems less likely as the sticks used by the Puffins seemed dry and therefore unlikely to have released chemical substances. As regards the former hypothesis, the absence, so far, of reports of wild Birds using sticks as mechanical tools for preening could be due to a lack of need for this behaviour, as Birds can access most of their body with their beak. Nonetheless, reports of captive Parrots scratching with stick-like objects suggest this behaviour may exist in the wild but has remained unreported due to its rarity. The case of the Puffins may reflect a specific ecological need which only occurs in some circumstances. For example, Puffins suffer from Seabird Ticks, Ixodes uriae, which were particularly abundant on Grimsey Island in the summer of 2018. The stick may have helped with scratching or dislodging them, perhaps more effectively than the beak. In either case, mechanical or chemical application, investigating the role of parasites as potential drivers of the emergence of bodycare-related tool use, for example by testing whether tool use prevalence correlates with parasite load in populations, would be an interesting avenue for future research.

Thus, Fayet et al.'s observations indicate that wild Birds may have a wider tool-use repertoire for physical self-maintenance than current evidence suggests. The fact that several species of Parrots showed this behaviour in captivity further supports this hypothesis, and the pattern of such behaviour having been observed multiple times independently and in different species may suggest that the behaviour may not simply be an artifact of captivity. Furthermore, the similarity of tool use between Birds and Primates has been mainly discussed in the context of feeding to date. Fayet et al.'s findings highlight the need to broaden this discussion to include other functions such as physical maintenance.

More broadly, the findings provide evidence of true tool use in a Seabird. This suggests tool use is rare in this group, but can no longer be considered absent. Tool use is present in a small number of Bird species (less than 1% of known genera) and is mostly related to feeding, presumably because of the high fitness gains reaped by accessing concealed food sources, especially when these are more profitable than non-concealed ones. Seabirds feed at sea, mainly on Fish, and have evolved unparallelled abilities to dive, swim, and catch prey underwater. The ocean seems an unlikely setting for Seabirds to evolve tool use, not least because of the lack of objects to use as tools and of concealed food sources in the water. Tool use, indeed, seems even rarer in aquatic animals than terrestrial ones. Seabirds only visit land to breed, which limits the opportunity for tool use and could favour its use for non-foraging purposes like courtship or physical maintenance. Such behaviours may also remain unreported because Seabirds are difficult to observe: They spend most of their time at sea, underground, or on inaccessible cliffs, and many are nocturnal. Fayet et al.'s finding of another physical maintenance tool-use behaviour in wild Birds besides anting suggests that tool use can emerge without strong selective pressure to obtain resources.

The fact that the two observations occurred on distant populations also raises interesting questions regarding their implications for the Birds’ underlying cognition. One possibility is that the behaviour arose by independent behavioural innovations as flexible problem solving by the Puffins observed, or that they socially learned this behaviour from other innovators. Alternatively, the behaviour could have a genetic component (in that it appears along a fixed developmental pathway without the need for innovation), present in both populations but rarely exhibited. Currently there is no way to distinguish between these scenarios; careful experimentation and information on the Birds’ history of interactions with sticks and conspecifics may reveal the extent to which stick use represents behavioural innovation and has the potential for social transmission. The propensity for behavioural innovation has been shown to increase with relative brain size in Birds and Primates. Seabirds’ relative brain size is comparatively small and they are not generally described as possessing sophisticated cognitive abilities. However, they feed in patchy, unpredictable environments, where they must integrate multiple sources of physical and social information to make complex decisions in space and time. Solving such problems requires behavioural flexibility and skills in multiple domains including learning, memory, and planning, also evidenced by high levels of fidelity in migration and foraging routes in numerous species. As such, Seabirds’ cognitive capacities may have been considerably underestimated. The fact that to date the only other Birds seen scratching with a stick are Parrots, which are prolific tool users and problem solvers, supports this hypothesis.

In summary, our discovery of another type of tool use in wild Birds, outside of the Passeriform order where most avian tool use is known to occur, and of a form so far restricted in the wild to Primates and Elephants, highlights the importance of widening the discussion on the evolution of animal tool use to a broader framework. While efforts to identify a single unifying driver for the emergence of all tool use are unlikely to succeed, a more complete picture of the range of contexts and taxa in which tool use occurs will allow behavioural scientists to break the phenomenon down into more meaningful categories for analysis. Fayet et al. therefore encourage researchers to include species not traditionally considered as good candidates for tool use and to report unusual behaviours across species. Their finding also warrants further studies on Seabird cognition, a topic almost entirely unstudied but clearly rife with opportunity for future research.

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1 comment:

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