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Funding: Biotechnology and Biological Sciences Research Council (BBSRC) (Grants BB/G023913/1 and BB/G023913/2 to C.R., and studentship to B.C.K.), the School of Biology at the University of St Andrews (studentships to M.P.S. and B.C.K.), and the Leverhulme Trust (Grant RPG-2015-273 to P.M.H.). 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. Publisher PDF

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Halimubieke, Naerhulan et al., When individuals breed more than once, parents are faced with the choice of whether to re-mate with their old partner or divorce and select a new mate. Evolutionary theory predicts that, following successful reproduction with a given partner, that partner should be retained for future reproduction. However, recent work in a polygamous bird, has instead indicated that successful parents divorced more often than failed breeders (Halimubieke et al. in Ecol Evol 9:10734–10745, 2019), because one parent can beneft by mating with a new partner and reproducing shortly after divorce. Here we investigate whether successful breeding predicts divorce using data from 14 well-monitored populations of plovers (Charadrius spp.). We show that successful nesting leads to divorce, whereas nest failure leads to retention of the mate for follow-up breeding. Plovers that divorced their partners and simultaneously deserted their broods produced more ofspring within a season than parents that retained their mate. Our work provides a counterpoint to theoretical expectations that divorce is triggered by low reproductive success, and supports adaptive explanations of divorce as a strategy to improve individual reproductive success. In addition, we show that temperature may modulate these costs and benefts, and contribute to dynamic variation in patterns of divorce across plover breeding systems

Aim: Parental care improves the survival of offspring and therefore has a major impact on reproductive success. It is increasingly recognized that coordinated biparental care is necessary to ensure the survival of offspring in hostile environments, but little is known about the influence of environmental fluctuations on parental cooperation. Assessing the impacts of environmental stochasticity, however, is essential for understanding how populations will respond to climate change and the associated increasing frequencies of extreme weather events. Here we investigate the influence of environmental stochasticity on biparental incubation in a cosmopolitan ground-nesting avian genus. Location: Global. Methods: We assembled data on biparental care in 36 plover populations (Charadrius spp.) from six continents, collected between 1981 and 2012. Using a space-for-time approach we investigate how average temperature, temperature stochasticity (i.e. year-to-year variation) and seasonal temperature variation during the breeding season influence parental cooperation during incubation. Results: We show that both average ambient temperature and its fluctuations influence parental cooperation during incubation. Male care relative to female care increases with both mean ambient temperature and temperature stochasticity. Local climatic conditions explain within-species population differences in parental cooperation, probably reflecting phenotypic plasticity of behaviour. Main conclusions: The degree of flexibility in parental cooperation is likely to mediate the impacts of climate change on the demography and reproductive behaviour of wild animal populations.

Summary Recent research shows that New Caledonian crows can incorporate information from researcher-made objects into objects they subsequently manufacture. This ‘mental template matching’ is one of several possible — mutually compatible — mechanisms for the cultural transmission of tool designs among wild crows.

This project was funded through a BBSRC David Phillips Fellowship (BB/G023913/2 to C.R.), and a PhD studentship by the BBSRC and the University of St Andrews (to B.K.). Funding for the ‘Alalā conservation breeding programme was provided by the U.S. Fish and Wildlife Service, State of Hawai‘i Division of Forestry and Wildlife, Moore Family Foundation, several anonymous donors, and San Diego Zoo Global. 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. Publisher PDF

The study was funded through a BBSRC David Phillips Fellowship (grant BB/G023913/2 to C.R.), and PhD studentships from the BBSRC (B.K.) and JASSO (S.S.). 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. Postprint

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1,2,3,4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions1,5, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators6,7,8,9,10. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring)6,7,8,9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5,6,7,9. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1–19 h, whereas period length—the time in which a parent’s probability to incubate cycles once between its highest and lowest value—varied from 6–43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light–dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity5,6,7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms., The study was supported by the Max Planck Society (to B.K.). M.B. is a PhD student in the International Max Planck Research School for Organismal Biology.

Funding from the Biotechnology and Biological Sciences Research Council, UK (BBSRC; grant BB/G023913/2 to C.R., and studentship to B.C.K.), the University of St Andrews (C.R.), JASSO (S.S.), and the Royal Society of London (M.B.M.). Funding for thecaptive ‘Alala propagation programme was provided by the U.S. Fish and Wildlife Service, Hawai‘i Division of Forestry and Wildlife, Moore Family Foundation, Marisla Foundation, several anonymous donors, and San Diego Zoo Global. Only a handful of bird species are known to use foraging tools in the wild1. Amongst them, the New Caledonian crow (Corvus moneduloides) stands out with its sophisticated tool-making skills2, 3. 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 comparisons4. Here we show that another tropical corvid, the ‘Alalā (C. hawaiiensis; Hawaiian crow), is a highly dexterous tool user. Although the ‘Alalā became extinct in the wild in the early 2000s, and currently survives only in captivity5, 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. ‘Alalā and New Caledonian crows evolved in similar environments on remote tropical islands, yet are only distantly related6, 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 risk4, 7. 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. Postprint

Funded through a BBSRC David Phillips Fellowship (BB/G023913/1 and /2 to C.R.), and three PhD studentships (JASSO to S.S.; University of St Andrews to J.v.d.W.; BBSRC and University of St Andrews to B.K.). ‘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 lab-based research into the cognitive capacities of non-human animals. Publisher PDF

Bursts of speciation have followed colonization of remote oceanic islands by diverse taxa, a process evidenced by island endemics around the world. The present study explores whether the Malvinas – Falkland Islands (MFI), a relatively understudied archipelago off the South Atlantic coast of Patagonia, harbour endemic genetic lineages of passerine birds. Nine passerine species nest regularly in the MFI (Cinclodes antarcticus, Muscisaxicola maclovianus, Troglodytes cobbi, Cistothorus platensis, Turdus falcklandii, Anthus correndera, Melanodera melanodera, Sturnella loyca, and Carduelis barbata). Mitochondrial DNA (cytochrome c oxidase I sequences) are used to quantify and compare divergence between insular and continental populations, finding genetic patterns to vary across these nine species. Most MFI passerines do not show significant genetic differentiation from continental populations, whereas C. platensis, M. melanodera, and T. falcklandii are modestly diverged. Finally, T. cobbi differes markedly from its closest continental relative Troglodytes aedon, a result that is confirmed using nuclear and vocal data. The study also identifies broadly divergent lineages within continental populations of C. platensis and T. aedon. Taken together, these results suggest that the land bird populations of the MFI were established at different times. Troglodytes cobbi is the oldest MFI land bird, splitting from continental T. aedon during the Great Patagonian Glaciation of the Pleistocene. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••.

New Caledonian (NC) crows Corvus moneduloides are the most prolific avian tool users. In the wild, they use at least three distinct tool types to extract invertebrate prey from deadwood and vegetation, with some of their tools requiring complex manufacture, modification and/or deployment. Experiments with captive-bred, hand-raised NC crows have demonstrated that the species has a strong genetic predisposition for basic tool use and manufacture, suggesting that this behaviour is an evolved adaptation. This view is supported by recent stable-isotope analyses of the diets of wild crows, which revealed that tool use provides access to highly profitable hidden prey, with preliminary data indicating that parents preferentially feed their offspring with tool-derived food. Building on this work, our review examines the possible evolutionary origins of these birds' remarkable tool-use behaviour. Whilst robust comparative analyses are impossible, given the phylogenetic rarity of animal tool use, our examination of a wide range of circumstantial evidence enables a first attempt at reconstructing a plausible evolutionary scenario. We suggest that a common ancestor of NC crows, originating from a (probably) non-tool-using South-East Asian or Australasian crow population, colonised New Caledonia after its last emersion several million years ago. The presence of profitable but out-of-reach food, in combination with a lack of direct competition for these resources, resulted in a vacant woodpecker-like niche. Crows may have possessed certain behavioural and/or morphological features upon their arrival that predisposed them to express tool-use rather than specialised prey-excavation behaviour, although it is possible that woodpecker-like foraging preceded tool use. Low levels of predation risk may have further facilitated tool-use behaviour, by allowing greater expenditure of time and energy on object interaction and exploration, as well as the evolution of a 'slow' life-history, in which prolonged juvenile development enables acquisition of complex behaviours. Intriguingly, humans may well have influenced the evolution of at least some of the species' tool-oriented behaviours, via their possible introduction of candlenut trees together with the beetle larvae that infest them. Research on NC crows' tool-use behaviour in its full ecological context is still in its infancy, and we expect that, as more evidence accumulates, some of our assumptions and predictions will be proved wrong. However, it is clear from our analysis of existing work, and the development of some original ideas, that the unusual evolutionary trajectory of NC crows is probably the consequence of an intricate constellation of interplaying factors.

The widespread invasive rodents Rattus norvegicus, R. rattus, R. exulans and Mus musculus have been implicated in the decline and extinction of hundreds of island endemic vertebrates, but their effects on island invertebrates are less well-known. Here I present the first global review of the subject, which confirms that large-bodied invertebrates are most at risk from these rodents, and that although a disproportionate number of studies (69%) are from New Zealand, rodent-invertebrate impacts are geographically widespread. Mechanisms of impact are both direct (mediated by predation) and indirect (involving intermediary species). Some studies also suggest knock-on effects on ecosystem properties, and given the diverse ecological functions of invertebrates (as detritivores, primary consumers, predators, prey and pollinators), I suggest that an understanding of the interactions between invasive rodents and invertebrates in island ecosystems is essential for effective conservation management. Currently many reported impacts are unquantified, come from uncontrolled and unreplicated designs, or rely on time-series with inadequate baseline data. In addition to basic improvements in study design, this review highlights a need for studies which investigate mechanisms of impact, or impacts across trophic levels.

The relative contributions of males and females to incubation, and the diel schedules by which incubation is shared, are important breeding system traits. We used infra-red sensitive cameras to record incubation patterns at 13 nests of the Two-banded Plover Charadrius falklandicus in the Falkland Islands during both day and night. Because predation risk can affect incubation behaviour, we also recorded the diel pattern of nest predation in the wider study population. We found high nest attendance, female-biased incubation, and strong diel sex-roles, with females incubating during the day and males at night. We also found that incubation intermissions tended to be short but frequent, and were correlated strongly with the diel pattern of nest predations which occurred exclusively in the daylight hours (probably due to the absence of terrestrial mammals from the study site). Our results suggest that sex-roles are unusually strict in the Two-banded Plover, and that these strict sex-roles lead to inequality in incubation sharing and the level of exposure to sources of energetic cost such as disturbance by nest predators.

Nonlethal disturbance can impose fitness costs, particularly during sensitive life history stages such as reproduction. Prey animals are thus expected to assess the costs and benefits of expressing antipredator behavior in different circumstances and to respond optimally according to the perceived risk of predation. One prediction of this hypothesis is that the response to nonlethal disturbance should be elevated when the risk of predation is high, although few studies have tested this prediction with respect to the distribution of actual predators in nature. We used landscape-level variation in the distribution of large mammalian predators (feral cats) to investigate antipredator behavior in a small breeding shorebird, the Two-banded Plover Charadrius falklandicus .W e used 8 sites in the Falkland Islands and Argentina and measured the flushing distances of incubating Two-banded Plovers in response to a controlled human approach to the nest. We found that flushing distances were increased at sites where mammalian predators were present and decreased where exposure to humans was high. These effects were additive, and we interpret them as the effects of generalization and habituation, respectively. Key words: antipredator behavior, feral cats, human disturbance, introduced predators, natural experiment, nest predation, predation risk, shorebird. [Behav Ecol]

This study was funded through a BBSRC David Phillips Fellowship (BB/G023913/2; C.R.), studentships from JASSO (S.S.; L12126010025) and BBSRC/University of St Andrews (B.C.K.), and a JSPS overseas research fellowship (S.S.; H28/1018). 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]. Postprint

The ability to attend to the functional properties of foraging tools should affect energy-intake rates, fitness components and ultimately the evolutionary dynamics of tool-related behaviour. New Caledonian crows Corvus moneduloides use three distinct tool types for extractive foraging: non-hooked stick tools, hooked stick tools and tools cut from the barbed edges of Pandanus spp. leaves. The latter two types exhibit clear functional polarity, because of (respectively) a single terminal, crow-manufactured hook and natural barbs running along one edge of the leaf strip; in each case, the ‘hooks’ can only aid prey capture if the tool is oriented correctly by the crow during deployment. A previous experimental study of New Caledonian crows found that subjects paid little attention to the barbs of supplied (wide) pandanus tools, resulting in non-functional tool orientation during foraging. This result is puzzling, given the presumed fitness benefits of consistently orienting tools functionally in the wild. We investigated whether the lack of discrimination with respect to (wide) pandanus tool orientation also applies to hooked stick tools. We experimentally provided subjects with naturalistic replica tools in a range of orientations and found that all subjects used these tools correctly, regardless of how they had been presented. In a companion experiment, we explored the extent to which normally co-occurring tool features (terminal hook, curvature of the tool shaft and stripped bark at the hooked end) inform tool-orientation decisions, by forcing birds to deploy ‘unnatural’ tools, which exhibited these traits at opposite ends. Our subjects attended to at least two of the three tool features, although, as expected, the location of the hook was of paramount importance. We discuss these results in the context of earlier research and propose avenues for future work.

Maternal effects arise when a mother's phenotype or the environment she experiences influences the phenotype of her progeny. Most studies of adaptive maternal effects are a "snapshot" of a mother's lifetime offspring provisioning and do not generally consider the effects of earlier siblings on those produced later. Here we show that in soil mites, offspring provisioning strategies are dynamic, changing from an emphasis on egg number in young females to egg size in older females. This pattern may be adaptive if it increases the survival of younger offspring that must compete with older, larger siblings. The dynamic shift in egg provisioning was greater in high-food environments in which females lived longer, creating increasing asymmetry in offspring competitive abilities. Females reared in isolation and in the presence of a high-density colony had identical provisioning strategies, suggesting that, unlike males in this species, females do not use pheromones to assess colony size. Our findings suggest that the adaptive significance of maternal effects may be misinterpreted when studies consider only a snapshot of a female's offspring provisioning strategy or when components of the offspring provisioning strategy are studied in isolation.

Growing interest in the structure and dynamics of animal social networks has stimulated major advances [1], [2] and [3], but recording reliable association data for wild populations has remained challenging. While animal-borne ‘proximity’ tags have been available for some time [4], earlier devices were comparatively heavy, had limited detection ranges and/or necessitated recovery for data retrieval. We have developed wireless digital transceiver technology (‘Encounternet') that enables automated mapping of social networks in wild birds, yielding datasets of unprecedented size, quality and spatio-temporal resolution. Miniature, animal-borne tags record the proximity and duration of bird encounters, and periodically transfer logs to a grid of fixed receiver stations, from which datasets can be downloaded remotely for real-time analysis. We used our system to chart social associations in New Caledonian crows Corvus moneduloides [5] and [6]. Analysis of ca. 28,000 encounter logs for 34 crows over a 7-day period reveals a substantial degree of close-range association between non-family birds, demonstrating the potential for horizontal and oblique information exchange.