The significance of building behavior in the evolution of animal architecture

This work wassupported by Biotechnology and Biological Sciences Research Council Discovery Fellowship (BB/S01019X/1) to S.S.Animals make a diverse array of architectures including nests, bowers, roosts, traps, and tools. Much of the research into animal architecture has focused on the analysis of physical properties such as the dimensions and material of the architectures, rather than the behavior responsible for creating these architectures. However, the relationship between the architecture itself and the construction behavior that built it is not straightforward, and overlooking behavior risks obtaining an incomplete or even misleading picture of how animal architecture evolves. Here we review data about animal architectures broadly, with a particular focus on building by birds and social insects. We then highlight three ways in which a better understanding of building behavior could benefit the study of animal architecture: by clarifying how behavior leads to physical properties; by examining the costs and benefits of building behavior; and by determining the role of learning and how this interacts with selection on behavior. To integrate questions about building behavior alongside those about architectures, we propose a framework inspired by Niko Tinbergen's four questions, examining the mechanistic, ontogenetic, phylogenetic, and functional basis of animal building. By integrating the study of behavior and architecture across levels of analysis, we can gain a more holistic view of the behavior-architecture interactions, and a better understanding of how behavior, cognition, and evolution interact to produce the diversity seen in animal architecture.Publisher PDFPeer reviewe

Object manipulation without hands

Funding: This work was supported by BBSRC Discovery Fellowship (BB/S01019X/1) to S.S.Our current understanding of manipulation is based on primate hands, resulting in a detailed but narrow perspective of ways to handle objects. Although most other animals lack hands, they are still capable of flexible manipulation of diverse objects, including food and nest materials, and depend on dexterity in object handling to survive and reproduce. Birds, for instance, use their bills and feet to forage and build nests, while insects carry food and construct nests with their mandibles and legs. Bird bills and insect mandibles are much simpler than a primate hand, resembling simple robotic grippers. A better understanding of manipulation in these and other species would provide a broader comparative perspective on the origins of dexterity. Here we contrast data from primates, birds and insects, describing how they sense and grasp objects, and the neural architectures that control manipulation. Finally, we outline techniques for collecting comparable manipulation data from animals with diverse morphologies and describe the practical applications of studying manipulation in a wide range of species, including providing inspiration for novel designs of robotic manipulators.PostprintPeer reviewe

Seasonal contrasts in individual consistency of oriental honey buzzards' migration

Funding: This project was supported by the Ministry of the Environment in Japan, and the Japan Society for the Promotion of Science Overseas Research Fellowship (to S.S.: H28/1018).Individual consistency in migration can shine light on the mechanisms of migration. Most studies have reported that birds are more consistent in the timing than in the routes or stopover sites during migration, but some specialist species showed the opposite patterns, being more consistent in spatial than temporal aspects of migration. One possible explanation for this contrast is that specialists rely on particular food or habitat resources, which restrict the migratory routes they can take, leading to high spatial consistency. If this is the case, the effect of specialist foraging should become apparent only when birds forage, instead of fasting and flying continuously. To test this effect, we analysed individual consistency in migration of the oriental honey buzzard (Pernis ptilorhynchus), a specialist raptor that feeds on honeybees and wasps, using a long-term tracking dataset. As honey buzzards make extended stopovers during which they forage in spring but not in autumn, the spatial consistency should be higher in spring than in autumn. Honey buzzards were highly consistent in both their migratory routes and stopover sites in Southeast Asia, but only during spring migration. Our results highlight an important link between species' migratory consistency and foraging ecology.PostprintPeer reviewe

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

The study was funded through a BBSRC David Phillips Fellowship (grants BB/G023913/1 and BB/G023913/2 to CR) and doctoral studentships from the BBSRC (BK), JASSO (SS), and the School of Biology, University of St Andrews (JvdW).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.Publisher PDFPeer reviewe

Space, the original frontier

S.S. was supported by BBSRC Discovery Fellowship (BB/S01019X/1).Over fifty years of work on animal cognition, enthusiasms for different topics can wax and wane. Interest in spatial cognition, once popular, has more recently waned. Some of this change, however, is only apparent, as research on spatial cognition continues to evolve and produce new scientific innovations. Indeed, recent technological developments has enabled us to now address questions raised from classic early studies. Here we review several key examples where past and present research approaches have intersected to provide new answers to old questions concerning spatial memory in food-storing birds and other laboratory animals, navigation in birds and insects, and spatial cognition in wild hummingbirds.Publisher PDFPeer reviewe

Anthropogenic nest material use in a global sample of birds

As humans increasingly modify the natural world, many animals have responded by changing their behaviour. Understanding and predicting the extent of these responses is a key step in conserving these species. For example, the tendency for some species of birds to incorporate anthropogenic items—particularly plastic material—into their nests is of increasing concern, as in some cases, this behaviour has harmful effects on adults, young and eggs. Studies of this phenomenon, however, have to date been largely limited in geographic and taxonomic scope. To investigate the global correlates of anthropogenic (including plastic) nest material use, we used Bayesian phylogenetic mixed models and a data set of recorded nest materials in 6147 species of birds. We find that, after controlling for research effort and proximity to human landscape modifications, anthropogenic nest material use is correlated with synanthropic (artificial) nesting locations, breeding environment and the number of different nest materials the species has been recorded to use. We also demonstrate that body mass, range size, conservation status and brain size do not explain variation in the recorded use of anthropogenic nest materials. These results indicate that anthropogenic materials are more likely to be included in nests when they are more readily available, as well as potentially by species that are more flexible in their nest material choice

Beak shape and nest material use in birds

This work was supported by a BBSRC Discovery Fellowship (grant no. BB/S01019X/1); the John Templeton Foundation (grant no. 60501); and the European Research Council (grant no. 788203).The evolution of behaviour can both influence, and be influenced by, morphology. Recent advances in methods and data availability have facilitated broad-scale investigations of physical form and behavioural function in many contexts, but the relationship between animal morphology and object manipulation-particularly objects used in construction-remains largely unknown. Here, we employ a new global database of nest materials used by 5924 species of birds together with phylogenetically informed random forest models to evaluate the link between beak shape and these nest-building materials. We find that beak morphology, together with species diet and access to materials, can predict nest-material use above chance and with high accuracy (68-97%). Much of this relationship, however, is driven by phylogenetic signal and sampling biases. We therefore conclude that while variation in nest material use is linked with that of beak shape across bird species, these correlations are modulated by the ecological context and evolutionary history of these species.Publisher PDFPeer reviewe

Tool bending in New Caledonian crows

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 PDFPeer reviewe

Causes and consequences of tool shape variation in New Caledonian crows

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].PostprintPeer reviewe

Discovery of species-wide tool use in the Hawaiian crow

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.PostprintPeer reviewe