RESUMEN
Many mutualisms are exploited by third-party species, which benefit without providing anything in return. Exploitation can either destabilize or promote mutualisms, via mechanisms that are highly dependent on the ecological context. Here we study a remarkable bird-human mutualism, in which wax-eating greater honeyguides (Indicator indicator) guide humans (Homo sapiens) to wild bees' nests, in an exchange of knowledge about the location of nests for access to the wax combs inside. We test whether the depletion of wax by mammalian and avian exploiter species either threatens or stabilizes the mutualism. Using camera traps, we monitored feeding visits to wax comb made available following honey harvests. We found that greater honeyguides face competition for wax from conspecifics and nine exploiter species, five of which were not previously known to consume wax. Our results support the hypothesis that heterospecific exploiters stabilize the mutualism, because wax depletion by these competitors probably limits feeding opportunities for conspecific exploiters, favouring the early-arriving individual that guided humans to the bees' nest. These findings highlight the importance of the ecological context of species interactions and provide further evidence for how mutualisms can persist because of, and not in spite of, exploitation by third-party species.
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Miel , Simbiosis , Humanos , Abejas , Animales , Ceras , Aves , MamíferosRESUMEN
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.
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Código de Barras del ADN Taxonómico , Comportamiento del Uso de la Herramienta/fisiología , Animales , Cuervos , ADN de Plantas/genética , Comportamiento de Nidificación/fisiología , Filogenia , Estructuras de las Plantas/anatomía & histología , Estructuras de las Plantas/clasificación , Estructuras de las Plantas/genéticaRESUMEN
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 benefit 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 offspring 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 benefits, and contribute to dynamic variation in patterns of divorce across plover breeding systems.
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Evolución Biológica , Charadriiformes/fisiología , Reproducción/fisiología , Conducta Sexual Animal/fisiología , Animales , Cruzamiento , Divorcio , Femenino , Masculino , ApareamientoRESUMEN
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.
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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.
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Comportamiento del Uso de la HerramientaRESUMEN
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.
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Cuervos/fisiología , Conducta Alimentaria , Comportamiento del Uso de la Herramienta , Animales , Femenino , MasculinoRESUMEN
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].
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Cuervos/fisiología , Comportamiento del Uso de la Herramienta , Factores de Edad , Animales , Conducta Alimentaria , Femenino , MasculinoRESUMEN
'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.
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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.
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The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. 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). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization 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 captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.
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Charadriiformes/fisiología , Comportamiento de Nidificación/fisiología , Periodicidad , Conducta Predatoria , Animales , Evolución Biológica , Charadriiformes/clasificación , Ritmo Circadiano , Señales (Psicología) , Ambiente , Conducta Alimentaria , Femenino , Masculino , Fotoperiodo , Reproducción , Especificidad de la Especie , Inanición/veterinaria , Factores de Tiempo , Cigoto/crecimiento & desarrolloRESUMEN
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.
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Cuervos/fisiología , Comportamiento del Uso de la Herramienta , Envejecimiento , Animales , Animales de Zoológico/fisiología , Evolución Biológica , Cognición , Cuervos/clasificación , Femenino , Hawaii , Masculino , Filogenia , Especificidad de la EspecieRESUMEN
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.
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Cuervos/fisiología , Comportamiento del Uso de la Herramienta , Animales , Evolución Biológica , Nueva CaledoniaRESUMEN
Social-network dynamics have profound consequences for biological processes such as information flow, but are notoriously difficult to measure in the wild. We used novel transceiver technology to chart association patterns across 19 days in a wild population of the New Caledonian crow--a tool-using species that may socially learn, and culturally accumulate, tool-related information. To examine the causes and consequences of changing network topology, we manipulated the environmental availability of the crows' preferred tool-extracted prey, and simulated, in silico, the diffusion of information across field-recorded time-ordered networks. Here we show that network structure responds quickly to environmental change and that novel information can potentially spread rapidly within multi-family communities, especially when tool-use opportunities are plentiful. At the same time, we report surprisingly limited social contact between neighbouring crow communities. Such scale dependence in information-flow dynamics is likely to influence the evolution and maintenance of material cultures.
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Cuervos , Difusión de la Información , Conducta Social , Aprendizaje Social , Comportamiento del Uso de la Herramienta , Animales , Simulación por Computador , AmbienteRESUMEN
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.
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Cuervos/fisiología , Conducta Alimentaria , Comportamiento del Uso de la Herramienta , Animales , Evolución Biológica , Femenino , MasculinoRESUMEN
Growing interest in the structure and dynamics of animal social networks has stimulated efforts to develop automated tracking technologies that can reliably record encounters in free-ranging subjects. A particularly promising approach is the use of animal-attached 'proximity loggers', which collect data on the incidence, duration and proximity of spatial associations through inter-logger radio communication. While proximity logging is based on a straightforward physical principle - the attenuation of propagating radio waves with distance - calibrating systems for field deployment is challenging, since most study species roam across complex, heterogeneous environments.In this study, we calibrated a recently developed digital proximity-logging system ('Encounternet') for deployment on a wild population of New Caledonian crows Corvus moneduloides. Our principal objective was to establish a quantitative model that enables robust post hoc estimation of logger-to-logger (and, hence, crow-to-crow) distances from logger-recorded signal-strength values. To achieve an accurate description of the radio communication between crow-borne loggers, we conducted a calibration exercise that combines theoretical analyses, field experiments, statistical modelling, behavioural observations, and computer simulations.We show that, using signal-strength information only, it is possible to assign crow encounters reliably to predefined distance classes, enabling powerful analyses of social dynamics. For example, raw data sets from field-deployed loggers can be filtered at the analysis stage to include predominantly encounters where crows would have come to within a few metres of each other, and could therefore have socially learned new behaviours through direct observation. One of the main challenges for improving data classification further is the fact that crows - like most other study species - associate across a wide variety of habitats and behavioural contexts, with different signal-attenuation properties.Our study demonstrates that well-calibrated proximity-logging systems can be used to chart social associations of free-ranging animals over a range of biologically meaningful distances. At the same time, however, it highlights that considerable efforts are required to conduct study-specific system calibrations that adequately account for the biological and technological complexities of field deployments. Although we report results from a particular case study, the basic rationale of our multi-step calibration exercise applies to many other tracking systems and study species.
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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.
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Cuervos , Conducta Alimentaria , Comportamiento del Uso de la Herramienta , Animales , Distribución Binomial , Femenino , Masculino , Nueva Caledonia , Grabación en VideoRESUMEN
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.
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Evolución Biológica , Cuervos , Ambiente , Comportamiento del Uso de la Herramienta , Animales , Conducta Apetitiva , Nueva CaledoniaRESUMEN
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.