DNA barcoding identifies cryptic animal tool materials.

Some animals fashion tools or constructions out of plant materials to aid foraging, reproduction, self-maintenance, or protection. Their choice of raw materials can affect the structure and properties of the resulting artifacts, with considerable fitness consequences. Documenting animals' material preferences is challenging, however, as manufacture behavior is often difficult to observe directly, and materials may be processed so heavily that they lack identifying features. Here, we use DNA barcoding to identify, from just a few recovered tool specimens, the plant species New Caledonian crows (Corvus moneduloides) use for crafting elaborate hooked stick tools in one of our long-term study populations. The method succeeded where extensive fieldwork using an array of conventional approaches-including targeted observations, camera traps, radio-tracking, bird-mounted video cameras, and behavioral experiments with wild and temporarily captive subjects-had failed. We believe that DNA barcoding will prove useful for investigating many other tool and construction behaviors, helping to unlock significant research potential across a wide range of study systems.

Sexy tools: Individual differences in drumming tool shape.

Heinsohn et al. Proceedings of the Royal Society B, 290, 2023.1271, (2023) report that the choice of tool type (drumsticks or seed pods) and the shape of drumsticks manufactured by palm cockatoos differ among individuals. This variation does not seem to be culturally transmitted as no spatial correlation between proximity of display trees and tool shape was found.

Discovery of species-wide tool use in the Hawaiian crow.

Only a handful of bird species are known to use foraging tools in the wild. Amongst them, the New Caledonian crow (Corvus moneduloides) stands out with its sophisticated tool-making skills. Despite considerable speculation, the evolutionary origins of this species' remarkable tool behaviour remain largely unknown, not least because no naturally tool-using congeners have yet been identified that would enable informative comparisons. Here we show that another tropical corvid, the 'Alala (C. hawaiiensis; Hawaiian crow), is a highly dexterous tool user. Although the 'Alala became extinct in the wild in the early 2000s, and currently survives only in captivity, at least two lines of evidence suggest that tool use is part of the species' natural behavioural repertoire: juveniles develop functional tool use without training, or social input from adults; and proficient tool use is a species-wide capacity. 'Alala and New Caledonian crows evolved in similar environments on remote tropical islands, yet are only distantly related, suggesting that their technical abilities arose convergently. This supports the idea that avian foraging tool use is facilitated by ecological conditions typical of islands, such as reduced competition for embedded prey and low predation risk. Our discovery creates exciting opportunities for comparative research on multiple tool-using and non-tool-using corvid species. Such work will in turn pave the way for replicated cross-taxonomic comparisons with the primate lineage, enabling valuable insights into the evolutionary origins of tool-using behaviour.

Short-range hunters: exploring the function and constraints of water shooting in dwarf gouramis.

Ballistic predation is a rare foraging adaptation: in fishes, most attention has focused on a single genus, the archerfish, known to manipulate water to shoot down prey above the water surface. However, several gourami species also exhibit apparently similar 'shooting' behaviour, spitting water up to 5 cm above the surface. In a series of experiments, we explored the shooting behaviour and aspects of its significance as a foraging ability in the dwarf gourami (Trichogaster lalius). We investigated sex differences in shooting abilities to determine whether gourami shooting is related to the sex-specific bubble nest manufacture where males mix air and water at the surface to form bubbles. We found that, actually, both sexes were equally able to shoot and could learn to shoot a novel target. In a second experiment, we presented untrained gouramis with opportunities to shoot at live prey and found they successfully shot down both fruit flies and crickets. Finally, we explored the effect of target height on shooting performance to establish potential constraints of shooting as a foraging ability. The frequency of attempted shots and success of hitting targets decreased with height, whereas latency to shoot increased. We also observed that repeatable individual differences account for variation in these measures of shooting performance. Together, our results provide evidence that gourami shooting has a foraging function analogous to that of archerfish. Gourami shooting may serve as an example of convergent evolution and provide opportunities for comparative studies into the, as yet unexplored, ecology and evolution of shooting in fishes.

Raw-material selectivity in hook-tool-crafting New Caledonian crows.

Animals that manufacture foraging tools face the challenge of identifying suitable raw materials among a multitude of options. New Caledonian crows exhibit strong population-specific material preferences for the manufacture of hooked stick tools, but it is unknown how they identify their favourite plants. We investigated experimentally whether crows pay attention to the stems of plants (from which the tools are made) and/or their leaves (which are usually discarded during manufacture but may enable rapid and reliable species identification at a distance). Subjects were highly selective in choice trials with multiple plant species. Two additional treatments with experimental leaf-stem combinations revealed that birds can identify their preferred plant species by its stems alone, and possibly also its leaves. These findings encourage future experiments that investigate whether New Caledonian crows attend to features of the stem that are required for the production of efficient hooked stick tools. Our study provides one of the most detailed assessments to date of how non-human animals identify raw materials for tool manufacture.

Hook tool manufacture in New Caledonian crows: behavioural variation and the influence of raw materials.

BACKGROUND: New Caledonian crows use a range of foraging tools, and are the only non-human species known to craft hooks. Based on a small number of observations, their manufacture of hooked stick tools has previously been described as a complex, multi-stage process. Tool behaviour is shaped by genetic predispositions, individual and social learning, and/or ecological influences, but disentangling the relative contributions of these factors remains a major research challenge. The properties of raw materials are an obvious, but largely overlooked, source of variation in tool-manufacture behaviour. We conducted experiments with wild-caught New Caledonian crows, to assess variation in their hooked stick tool making, and to investigate how raw-material properties affect the manufacture process. RESULTS: In Experiment 1, we showed that New Caledonian crows' manufacture of hooked stick tools can be much more variable than previously thought (85 tools by 18 subjects), and can involve two newly-discovered behaviours: 'pulling' for detaching stems and bending of the tool shaft. Crows' tool manufactures varied significantly: in the number of different action types employed; in the time spent processing the hook and bending the tool shaft; and in the structure of processing sequences. In Experiment 2, we examined the interaction of crows with raw materials of different properties, using a novel paradigm that enabled us to determine subjects' rank-ordered preferences (42 tools by 7 subjects). Plant properties influenced: the order in which crows selected stems; whether a hooked tool was manufactured; the time required to release a basic tool; and, possibly, the release technique, the number of behavioural actions, and aspects of processing behaviour. Results from Experiment 2 suggested that at least part of the natural behavioural variation observed in Experiment 1 is due to the effect of raw-material properties. CONCLUSIONS: Our discovery of novel manufacture behaviours indicates a plausible scenario for the evolutionary origins, and gradual refinement, of New Caledonian crows' hooked stick tool making. Furthermore, our experimental demonstration of a link between raw-material properties and aspects of tool manufacture provides an alternative hypothesis for explaining regional differences in tool behaviours observed in New Caledonian crows, and some primate species.

Context-dependent 'safekeeping' of foraging tools in New Caledonian crows.

Several animal species use tools for foraging, such as sticks to extract embedded arthropods and honey, or stones to crack open nuts and eggs. While providing access to nutritious foods, these behaviours may incur significant costs, such as the time and energy spent searching for, manufacturing and transporting tools. These costs can be reduced by re-using tools, keeping them safe when not needed. We experimentally investigated what New Caledonian crows do with their tools between successive prey extractions, and whether they express tool 'safekeeping' behaviours more often when the costs (foraging at height), or likelihood (handling of demanding prey), of tool loss are high. Birds generally took care of their tools (84% of 176 prey extractions, nine subjects), either trapping them underfoot (74%) or storing them in holes (26%)--behaviours we also observed in the wild (19 cases, four subjects). Moreover, tool-handling behaviour was context-dependent, with subjects: keeping their tools safe significantly more often when foraging at height; and storing tools significantly more often in holes when extracting more demanding prey (under these conditions, foot-trapping proved challenging). In arboreal environments, safekeeping can prevent costly tool losses, removing a potentially important constraint on the evolution of habitual and complex tool behaviour.

Tool use promotes dental health.

Using tools increases foraging success in sea otters and protects their teeth from damage.

callsync: An R package for alignment and analysis of multi-microphone animal recordings.

To better understand how vocalisations are used during interactions of multiple individuals, studies are increasingly deploying on-board devices with a microphone on each animal. The resulting recordings are extremely challenging to analyse, since microphone clocks drift non-linearly and record the vocalisations of non-focal individuals as well as noise. Here we address this issue with callsync, an R package designed to align recordings, detect and assign vocalisations to the caller, trace the fundamental frequency, filter out noise and perform basic analysis on the resulting clips. We present a case study where the pipeline is used on a dataset of six captive cockatiels (Nymphicus hollandicus) wearing backpack microphones. Recordings initially had a drift of ~2 min, but were aligned to within ~2 s with our package. Using callsync, we detected and assigned 2101 calls across three multi-hour recording sessions. Two had loud beep markers in the background designed to help the manual alignment process. One contained no obvious markers, in order to demonstrate that markers were not necessary to obtain optimal alignment. We then used a function that traces the fundamental frequency and applied spectrographic cross correlation to show a possible analytical pipeline where vocal similarity is visually assessed. The callsync package can be used to go from raw recordings to a clean dataset of features. The package is designed to be modular and allows users to replace functions as they wish. We also discuss the challenges that might be faced in each step and how the available literature can provide alternatives for each step.

Is bin-opening in cockatoos leading to an innovation arms race with humans?

Foraging innovations can give wild animals access to human-derived food sources1. If these innovations spread, they can enable adaptive flexibility2 but also lead to human-wildlife conflicts3. Examples include crop-raiding elephants4 and long-tailed macaques that steal items from people to trade them back for food5. Behavioural responses by humans might act as a further driver on animal innovation2,6, even potentially leading to an inter-species 'innovation arms-race'7, yet this is almost entirely unexplored. Here, we report a potential case in wild, urban-living, sulphur-crested cockatoos (Cacatua galerita; henceforth cockatoos), where the socially-learnt behaviour of opening and raiding of household bins by cockatoos8 is met with increasingly effective and socially-learnt bin-protection measures by human residents.

ANIMAL-SPOT enables animal-independent signal detection and classification using deep learning.

Bioacoustic research spans a wide range of biological questions and applications, relying on identification of target species or smaller acoustic units, such as distinct call types. However, manually identifying the signal of interest is time-intensive, error-prone, and becomes unfeasible with large data volumes. Therefore, machine-driven algorithms are increasingly applied to various bioacoustic signal identification challenges. Nevertheless, biologists still have major difficulties trying to transfer existing animal- and/or scenario-related machine learning approaches to their specific animal datasets and scientific questions. This study presents an animal-independent, open-source deep learning framework, along with a detailed user guide. Three signal identification tasks, commonly encountered in bioacoustics research, were investigated: (1) target signal vs. background noise detection, (2) species classification, and (3) call type categorization. ANIMAL-SPOT successfully segmented human-annotated target signals in data volumes representing 10 distinct animal species and 1 additional genus, resulting in a mean test accuracy of 97.9%, together with an average area under the ROC curve (AUC) of 95.9%, when predicting on unseen recordings. Moreover, an average segmentation accuracy and F1-score of 95.4% was achieved on the publicly available BirdVox-Full-Night data corpus. In addition, multi-class species and call type classification resulted in 96.6% and 92.7% accuracy on unseen test data, as well as 95.2% and 88.4% regarding previous animal-specific machine-based detection excerpts. Furthermore, an Unweighted Average Recall (UAR) of 89.3% outperformed the multi-species classification baseline system of the ComParE 2021 Primate Sub-Challenge. Besides animal independence, ANIMAL-SPOT does not rely on expert knowledge or special computing resources, thereby making deep-learning-based bioacoustic signal identification accessible to a broad audience.

New Caledonian crows keep 'valuable' hooked tools safer than basic non-hooked tools.

The temporary storage and re-use of tools can significantly enhance foraging efficiency. New Caledonian crows in one of our study populations use two types of stick tools - hooked and non-hooked - which differ in raw material, manufacture costs, and foraging performance. Using a large sample of wild-caught, temporarily captive New Caledonian crows, we investigated experimentally whether individuals prefer one tool type over the other when given a choice and whether they take better care of their preferred tools between successive episodes of use, safely storing them underfoot or in nearby holes. Crows strongly preferred hooked stick tools made from Desmanthus virgatus stems over non-hooked stick tools. Importantly, this preference was also reflected in subsequent tool-handling behaviour, with subjects keeping hooked stick tools safe more often than non-hooked stick tools sourced from leaf litter. These results suggest that crows 'value' hooked stick tools, which are both costlier to procure and more efficient to use, more than non-hooked stick tools. Results from a series of control treatments suggested that crows altered their tool 'safekeeping' behaviour in response to a combination of factors, including tool type and raw material. To our knowledge, our study is the first to use safekeeping behaviour as a proxy for assessing how non-human animals value different tool types, establishing a novel paradigm for productive cross-taxonomic comparisons.

Innovation and geographic spread of a complex foraging culture in an urban parrot.

The emergence, spread, and establishment of innovations within cultures can promote adaptive responses to anthropogenic change. We describe a putative case of the development of a cultural adaptation to urban environments: opening of household waste bins by wild sulphur-crested cockatoos. A spatial network analysis of community science reports revealed the geographic spread of bin opening from three suburbs to 44 in Sydney, Australia, by means of social learning. Analysis of 160 direct observations revealed individual styles and site-specific differences. We describe a full pathway from the spread of innovation to emergence of geographic variation, evidencing foraging cultures in parrots and indicating the existence of cultural complexity in parrots. Bin opening is directly linked to human-provided opportunities, highlighting the potential for culture to facilitate behavioral responses to anthropogenic change.

Preliminary observations of tool-processing behaviour in Hawaiian crows Corvus hawaiiensis.

Very few animal species habitually make and use foraging tools. We recently discovered that the Hawaiian crow is a highly skilled, natural tool user. Most captive adults in our experiment spontaneously used sticks to access out-of-reach food from a range of extraction tasks, exhibiting a surprising degree of dexterity. Moreover, many birds modified tools before or during deployment, and some even manufactured tools from raw materials. In this invited addendum article, we describe and discuss these observations in more detail. Our preliminary data, and comparisons with the better-studied New Caledonian crow, suggest that the Hawaiian crow has extensive tool-modification and manufacture abilities. To chart the full extent of the species' natural tool-making repertoire, we have started conducting dedicated experiments where subjects are given access to suitable raw materials for tool manufacture, but not ready-to-use tools.

Hook innovation boosts foraging efficiency in tool-using crows.

The New Caledonian crow is the only non-human animal known to craft hooked tools in the wild, but the ecological benefit of these relatively complex tools remains unknown. Here, we show that crows acquire food several times faster when using hooked rather than non-hooked tools, regardless of tool material, prey type and extraction context. This implies that small changes to tool shape can strongly affect energy-intake rates, highlighting a powerful driver for technological advancement.

Causes and Consequences of Tool Shape Variation in New Caledonian Crows.

Hominins have been making tools for over three million years [1], yet the earliest known hooked tools appeared as recently as 90,000 years ago [2]. Hook innovation is likely to have boosted our ancestors' hunting and fishing efficiency [3], marking a major transition in human technological evolution. The New Caledonian crow is the only non-human animal known to craft hooks in the wild [4, 5]. Crows manufacture hooked stick tools in a multi-stage process, involving the detachment of a branch from suitable vegetation; "sculpting" of a terminal hook from the nodal joint; and often additional adjustments, such as length trimming, shaft bending, and bark stripping [4, 6, 7]. Although tools made by a given population share key design features [4, 6, 8], they vary appreciably in overall shape and hook dimensions. Using wild-caught, temporarily captive crows, we experimentally investigated causes and consequences of variation in hook-tool morphology. We found that bird age, manufacture method, and raw-material properties influenced tool morphology, and that hook geometry in turn affected crows' foraging efficiency. Specifically, hook depth varied with both detachment technique and plant rigidity, and deeper hooks enabled faster prey extraction in the provided tasks. Older crows manufactured tools of distinctive shape, with pronounced shaft curvature and hooks of intermediate depth. Future work should explore the interactive effects of extrinsic and intrinsic factors on tool production and deployment. Our study provides a quantitative assessment of the drivers and functional significance of tool shape variation in a non-human animal, affording valuable comparative insights into early hominin tool crafting [9].

Tool bending in New Caledonian crows.

'Betty' the New Caledonian crow astonished the world when she 'spontaneously' bent straight pieces of garden wire into hooked foraging tools. Recent field experiments have revealed that tool bending is part of the species' natural behavioural repertoire, providing important context for interpreting Betty's iconic wire-bending feat. More generally, this discovery provides a compelling illustration of how natural history observations can inform laboratory-based research into the cognitive capacities of non-human animals.

Strong between-site variation in New Caledonian crows' use of hook-tool-making materials.

Functional tool use requires the selection of appropriate raw materials. New Caledonian crows Corvus moneduloides are known for their extraordinary tool-making behaviour, including the crafting of hooked stick tools from branched vegetation. We describe a surprisingly strong between-site difference in the plant materials used by wild crows to manufacture these tools: crows at one study site use branches of the non-native shrub Desmanthus virgatus, whereas only approximately 7 km away, birds apparently ignore this material in favour of the terminal twigs of an as-yet-unidentified tree species. Although it is likely that differences in local plant communities drive this striking pattern, it remains to be determined how and why crows develop such strong site-specific preferences for certain raw materials.