Nest architecture influences host use by avian brood parasites and is shaped by coevolutionary dynamics.

Brood (social) parasites and their hosts exhibit a wide range of adaptations and counter-adaptations as part of their ongoing coevolutionary arms races. Obligate avian brood parasites are expected to use potential host species with more easily accessible nests, while potential hosts are expected to evade parasitism by building more concealed nests that are difficult for parasites to enter and in which to lay eggs. We used phylogenetically informed comparative analyses, a global database of the world's brood parasites, their host species, and the design of avian host and non-host nests (approx. 6200 bird species) to examine first, whether parasites preferentially target host species that build open nests and, second, whether host species that build enclosed nests are more likely to be targeted by specialist parasites. We found that species building more accessible nests are more likely to serve as hosts, while host species with some of the more inaccessible nests are targeted by more specialist brood parasites. Furthermore, evolutionary-transition analyses demonstrate that host species building enclosed nests frequently evolve to become non-hosts. We conclude that nest architecture and the accessibility of nests for parasitism represent a critical stage of the ongoing coevolutionary arms race between avian brood parasites and their hosts.

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.

Adding the neuro to cognition: from food storing to nest building.

Typically, investigations of animal cognition couple careful experimental manipulations with examination of the animal's behavioural responses. Sometimes those questions have included attempts to describe the neural underpinnings of the behavioural outputs. Over the past 25 years, behaviours that involve spatial learning and memory (such as navigation and food storing) has been one context in which such dual or correlated investigations have been both accessible and productive. Here I review some of that work and where it has led. Because of the wealth of data and insights gained from that work and song learning before it, it seems that it might also be useful to try to add some neurobiology to other systems in animal cognition. I finish then, with a description of recent work on the cognition and neurobiology of avian nest building. It is still relatively early days but asking questions about the cognition of nest building has already shown both neural correlates of nest building and that learning and memory play a much greater role in this behaviour than previously considered. While it is not yet clear how putting these components together will be synergistic, the examples of song learning and food storing provide encouragement. Perhaps this might be true for other behaviours too?

Global drivers of variation in cup nest size in passerine birds.

The size of a bird's nest can play a key role in ensuring reproductive success and is determined by a variety of factors. The primary function of the nest is to protect offspring from the environment and predators. Field studies in a number of passerine species have indicated that higher-latitude populations in colder habitats build larger nests with thicker walls compared to lower-latitude populations, but that these larger nests are more vulnerable to predation. Increases in nest size can also be driven by sexual selection, as nest size can act as a signal of parental quality and prompt differential investment in other aspects of care. It is unknown, however, how these microevolutionary patterns translate to a macroevolutionary scale. Here, we investigate potential drivers of variation in the outer and inner volume of open cup nests using a large dataset of nest measurements from 1117 species of passerines breeding in a diverse range of environments. Our dataset is sourced primarily from the nest specimens at the Natural History Museum (UK), complemented with information from ornithological handbooks and online databases. We use phylogenetic comparative methods to test long-standing hypotheses about potential macroevolutionary correlates of nest size, namely nest location, clutch size and variables relating to parental care, together with environmental and geographical factors such as temperature, rainfall, latitude and insularity. After controlling for phylogeny and parental body size, we demonstrate that the outer volume of the nest is greater in colder climates, in island-dwelling species and in species that nest on cliffs or rocks. By contrast, the inner cup volume is associated solely with average clutch size, increasing with the number of chicks raised in the nest. We do not find evidence that nest size is related to the length of parental care for nestlings. Our study reveals that the average temperature in the breeding range, along with several key life-history traits and proxies of predation threat, shapes the global interspecific variation in passerine cup nest size. We also showcase the utility of museum nest collections-a historically underused resource-for large-scale studies of trait evolution.

Size is relative: use of relational concepts by wild hummingbirds.

Rufous hummingbirds (Selasphorus rufus) will readily learn the location and the colour of rewarded flowers within their territory. But if these birds could apply a relational concept such as 'the larger flowers have more nectar', they could forego learning the locations of hundreds of individual flowers. Here, we investigated whether wild male territorial rufous hummingbirds might use 'larger than' and 'smaller than' relational rules and apply them to flowers of different sizes. Subjects were trained to feed consistently from one of two flowers. Although the flowers differed only in size, the reward was always contained in the same-size flower. The birds were then tested on a choice of two empty flowers: one of the familiar size and the other a novel size. Hummingbirds applied relational rules by choosing the flower that was of the correct relational size rather than visiting the flower of the size rewarded during training. The choices made by the hummingbirds were not consistent with alternative mechanisms such as peak shift or associative learning. We suggest that while hummingbirds are very good at remembering the spatial locations of rewarding flowers, they would be able to use relative rules when foraging in new and changing environments.

Involvement of the neural social behaviour network during social information acquisition in zebra finches (Taeniopygia guttata).

Female zebra finches Taeniopygia guttata will copy the novel foraging choice of males. The degree to which they do so, however, can vary considerably. Among-individual differences in social learning and their underlying neural pathways have received relatively little attention and remain poorly understood. Here, then, we allowed female zebra finches to observe live-streamed male demonstrators feeding from one of two novel-coloured feeders (social information acquisition phase). After this social information acquisition phase, we tested from which feeder the females preferred to feed to determine whether they copied the feeder choice of the male demonstrator (social learning test phase). We then examined the brains of these females for immediate early gene activity (c-fos) in the neural social behaviour network for the time during which they were observing the male feeding. Of the 12 regions and sub-regions in the brain examined we found only one weak correlation: greater copying was associated with lower activity in the bed nucleus of the stria terminalis, BSTmv. Future work should perhaps focus on neural activity that occurs during the stage in which there is evidence that animals have copied a demonstrator (i.e., social learning test phase in the current experiment) rather than during the period in which those animals observe that demonstrator (i.e., social information acquisition phase in the current experiment). What is clear is that the considerable emphasis on examining the behavioural component of social learning has not yet been accompanied by neural analyses.

Hummingbirds modify their routes to avoid a poor location.

Traplining, when animals repeat the order in which they visit a number of locations, is taxonomically widespread, but little is known about which factors influence the routes that animals follow. For example, as the quality of rewarding locations changes over time, foragers are expected to update their traplines, either to prioritize locations where the reward increases or to avoid locations that have ceased to be profitable. Here, we tested how traplining wild hummingbirds responded to increases or to decreases in the sucrose concentration of one of the flowers on their trapline. Hummingbirds did not change their trapline to visit the flower with the increased reward first, but by changing the order in which they visited flowers, they avoided a flower that contained a decreased reward. Depending on where along the trapline the reduced-content flower occurred, hummingbirds either changed the origin of their trapline or changed the direction in which they flew around their trapline. It may be that this asymmetric modification of foraging traplines is especially noticeable in risk-averse foragers, such as these territorial hummingbirds.

Object manipulation without hands.

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.

Estimating on the fly: The approximate number system in rufous hummingbirds (Selasphorus rufus).

When presented with resources that differ in quantity, many animals use a numerosity system to discriminate between them. One taxonomically widespread system is the approximate number system. This is a numerosity system that allows the rapid evaluation of the number of objects in a group and which is regulated by Weber's Law. Here we investigated whether wild, free-living rufous hummingbirds (Selasphorus rufus) possess an approximate number system. The hummingbirds were presented with two experiments. In the first we investigated whether hummingbirds spontaneously chose an array containing more flowers than an alternate array. In the second we asked whether the hummingbirds could learn to use numerosity as a cue to which of two arrays contained the better reward. The birds did not spontaneously prefer an array containing more flowers. After minimal training, however, they learned to choose the more numerous array and could differentiate between arrays of five and seven flowers. These data support the presence of an approximate number system in the rufous hummingbird. It seems plausible that having such a system would enable much more efficient foraging in this species.

Numerical ordinality in a wild nectarivore.

Ordinality is a numerical property that nectarivores may use to remember the specific order in which to visit a sequence of flowers, a foraging strategy also known as traplining. In this experiment, we tested whether wild, free-living rufous hummingbirds (Selasphorus rufus) could use ordinality to visit a rewarded flower. Birds were presented with a series of linear arrays of 10 artificial flowers; only one flower in each array was rewarded with sucrose solution. During training, birds learned to locate the correct flower independent of absolute spatial location. The birds' accuracy was independent of the rewarded ordinal position (1st, 2nd, 3rd or 4th), which suggests that they used an object-indexing mechanism of numerical processing, rather than a magnitude-based system. When distance cues between flowers were made irrelevant during test trials, birds could still locate the correct flower. The distribution of errors during both training and testing indicates that the birds may have used a so-called working up strategy to locate the correct ordinal position. These results provide the first demonstration of numerical ordinal abilities in a wild vertebrate and suggest that such abilities could be used during foraging in the wild.

Early-life adversity programs long-term cytokine and microglia expression within the HPA axis in female Japanese quail.

Stress exposure during prenatal and postnatal development can have persistent and often dysfunctional effects on several physiological systems, including immune function, affecting the ability to combat infection. The neuroimmune response is inextricably linked to the action of the hypothalamic-pituitary-adrenal (HPA) axis. Cytokines released from neuroimmune cells, including microglia, activate the HPA axis, while glucocorticoids in turn regulate cytokine release from microglia. Because of the close links between these two physiological systems, coupled with potential for persistent changes to HPA axis activity following developmental stress, components of the neuroimmune system could be targets for developmental programming. However, little is known of any programming effects of developmental stress on neuroimmune function. We investigated whether developmental stress exposure via elevated prenatal corticosterone (CORT) or postnatal unpredictable food availability had long-term effects on pro- (IL-1ß) and anti-inflammatory (IL-10) cytokine and microglia-dependent gene (CSF1R) expression within HPA axis tissues in a precocial bird, the Japanese quail (Coturnix japonica). Following postnatal stress, we observed increased IL-1ß expression in the pituitary gland, reduced IL-10 expression in the amygdala and hypothalamus, and reduced CSF1R expression within the hypothalamus and pituitary gland. Postnatal stress disrupted the ratio of IL-1ß:IL-10 expression within the hippocampus and hypothalamus. Prenatal stress only increased IL-1ß expression in the pituitary gland. We found no evidence for interactive or cumulative effects across life stages on basal cytokine and glia expression in adulthood. We show that postnatal stress may have a larger impact than elevated prenatal CORT on basal immunity in HPA-axis-specific brain regions, with changes in cytokine homeostasis and microglia abundance. These results provide evidence for postnatal programming of a pro-inflammatory neuroimmune phenotype at the expense of reduced microglia, which could have implications for central nervous system health and subsequent neuroimmune responses.

Social learning about construction behaviour via an artefact.

One source of public information may be the enduring products of others' behaviour, such as discarded tools or vacated nests. Here, we examined whether observation of a nest affects the material captive zebra finch males prefer when they construct their first nest. It does: for first-time nest construction, males that viewed only an empty cage preferred the colour of material each initially favoured but those males that had observed a pre-built nest of material of their non-preferred colour lost their material-colour preference altogether. Additionally, half of the males that viewed a nest were tested in an environment (the laboratory) different to that in which they were reared (an outdoor aviary). We had expected the aviary-reared (versus laboratory-reared) males would be more uncertain, and thus more likely to select material for their first nest that matched in colour to the colour of the 'demonstrated' nest-but this was not the case. The aviary-reared males did, however, tend to touch first the demonstrated colour of material more than did the laboratory-reared males. Together these results show that both observation of a nest and a change in environment can influence the material choices of novice builders. For naïve animal builders, then, construction artefacts can be information resources for learning about potential construction material.

Taking an insect-inspired approach to bird navigation.

Navigation is an essential skill for many animals, and understanding how animal use environmental information, particularly visual information, to navigate has a long history in both ethology and psychology. In birds, the dominant approach for investigating navigation at small-scales comes from comparative psychology, which emphasizes the cognitive representations underpinning spatial memory. The majority of this work is based in the laboratory and it is unclear whether this context itself affects the information that birds learn and use when they search for a location. Data from hummingbirds suggests that birds in the wild might use visual information in quite a different manner. To reconcile these differences, here we propose a new approach to avian navigation, inspired by the sensory-driven study of navigation in insects. Using methods devised for studying the navigation of insects, it is possible to quantify the visual information available to navigating birds, and then to determine how this information influences those birds' navigation decisions. Focusing on four areas that we consider characteristic of the insect navigation perspective, we discuss how this approach has shone light on the information insects use to navigate, and assess the prospects of taking a similar approach with birds. Although birds and insects differ in many ways, there is nothing in the insect-inspired approach of the kind we describe that means these methods need be restricted to insects. On the contrary, adopting such an approach could provide a fresh perspective on the well-studied question of how birds navigate through a variety of environments.

Adjusting foraging strategies: a comparison of rural and urban common mynas (Acridotheres tristis).

Establishment in urbanized environments is associated with changes in physiology, behaviour, and problem-solving. We compared the speed of learning in urban and rural female common mynas, Acridotheres tristis, using a standard visual discrimination task followed by a reversal learning phase. We also examined how quickly each bird progressed through different stages of learning, including sampling and acquisition within both initial and reversal learning, and persistence following reversal. Based on their reliance on very different food resources, we expected urban mynas to learn and reversal learn more quickly but to sample new contingencies for proportionately longer before learning them. When quantified from first presentation to criterion achievement, urban mynas took more 20-trial blocks to learn the initial discrimination, as well as the reversed contingency, than rural mynas. More detailed analyses at the level of stage revealed that this was because urban mynas explored the novel cue-outcome contingencies for longer, and despite transitioning faster through subsequent acquisition, remained overall slower than rural females. Our findings draw attention to fine adjustments in learning strategies in response to urbanization and caution against interpreting the speed to learn a task as a reflection of cognitive ability.

Social learning in nest-building birds: a role for familiarity.

It is becoming apparent that birds learn from their own experiences of nest building. What is not clear is whether birds can learn from watching conspecifics build. As social learning allows an animal to gain information without engaging in costly trial-and-error learning, first-time builders should exploit the successful habits of experienced builders. We presented first-time nest-building male zebra finches with either a familiar or an unfamiliar conspecific male building with material of a colour the observer did not like. When given the opportunity to build, males that had watched a familiar male build switched their material preference to that used by the familiar male. Males that observed unfamiliar birds did not. Thus, first-time nest builders use social information and copy the nest material choices when demonstrators are familiar but not when they are strangers. The relationships between individuals therefore influence how nest-building expertise is socially transmitted in zebra finches.

Effects of landmark distance and stability on accuracy of reward relocation.

Although small-scale navigation is well studied in a wide range of species, much of what is known about landmark use by vertebrates is based on laboratory experiments. To investigate how vertebrates in the wild use landmarks, we trained wild male rufous hummingbirds to feed from a flower that was placed in a constant spatial relationship with two artificial landmarks. In the first experiment, the landmarks and flower were 0.25, 0.5 or 1 m apart and we always moved them 3-4 m after each visit by the bird. In the second experiment, the landmarks and flower were always 0.25 m apart and we moved them either 1 or 0.25 m between trials. In tests, in which we removed the flower, the hummingbirds stopped closer to the predicted flower location when the landmarks had been closer to the flower during training. However, while the distance that the birds stopped from the landmarks and predicted flower location was unaffected by the distance that the landmarks moved between trials, the birds directed their search nearer to the predicted direction of the flower, relative to the landmarks, when the landmarks and flower were more stable in the environment. In the field, then, landmarks alone were sufficient for the birds to determine the distance of a reward but not its direction.

Three-dimensional space: locomotory style explains memory differences in rats and hummingbirds.

While most animals live in a three-dimensional world, they move through it to different extents depending on their mode of locomotion: terrestrial animals move vertically less than do swimming and flying animals. As nearly everything we know about how animals learn and remember locations in space comes from two-dimensional experiments in the horizontal plane, here we determined whether the use of three-dimensional space by a terrestrial and a flying animal was correlated with memory for a rewarded location. In the cubic mazes in which we trained and tested rats and hummingbirds, rats moved more vertically than horizontally, whereas hummingbirds moved equally in the three dimensions. Consistent with their movement preferences, rats were more accurate in relocating the horizontal component of a rewarded location than they were in the vertical component. Hummingbirds, however, were more accurate in the vertical dimension than they were in the horizontal, a result that cannot be explained by their use of space. Either as a result of evolution or ontogeny, it appears that birds and rats prioritize horizontal versus vertical components differently when they remember three-dimensional space.

Physical cognition: birds learn the structural efficacy of nest material.

It is generally assumed that birds' choice of structurally suitable materials for nest building is genetically predetermined. Here, we tested that assumption by investigating whether experience affected male zebra finches' (Taeniopygia guttata) choice of nest material. After a short period of building with relatively flexible string, birds preferred to build with stiffer string while those that had experienced a stiffer string were indifferent to string type. After building a complete nest with either string type, however, all birds increased their preference for stiff string. The stiffer string appeared to be the more effective building material as birds required fewer pieces of stiffer than flexible string to build a roofed nest. For birds that raised chicks successfully, there was no association between the material they used to build their nest and the type they subsequently preferred. Birds' material preference reflected neither the preference of their father nor of their siblings but juvenile experience of either string type increased their preference for stiffer string. Our results represent two important advances: (i) birds choose nest material based on the structural properties of the material; (ii) nest material preference is not entirely genetically predetermined as both the type and amount of experience influences birds' choices.

Wild hummingbirds rely on landmarks not geometry when learning an array of flowers.

Rats, birds or fish trained to find a reward in one corner of a small enclosure tend to learn the location of the reward using both nearby visual features and the geometric relationships of corners and walls. Because these studies are conducted under laboratory and thereby unnatural conditions, we sought to determine whether wild, free-living rufous hummingbirds (Selasphorus rufus) learning a single reward location within a rectangular array of flowers would similarly employ both nearby visual landmarks and the geometric relationships of the array. Once subjects had learned the location of the reward, we used test probes in which one or two experimental landmarks were moved or removed in order to reveal how the birds remembered the reward location. The hummingbirds showed no evidence that they used the geometry of the rectangular array of flowers to remember the reward. Rather, they used our experimental landmarks, and possibly nearby, natural landmarks, to orient and navigate to the reward. We believe this to be the first test of the use of rectangular geometry by wild animals, and we recommend further studies be conducted in ecologically relevant conditions in order to help determine how and when animals form complex geometric representations of their local environments.

What, where and when: deconstructing memory.

The ability of animals to remember the what, where and when of a unique past event is used as an animal equivalent to human episodic memory. We currently view episodic memory as reconstructive, with an event being remembered in the context in which it took place. Importantly, this means that the components of a what, where, when memory task should be dissociable (e.g. what would be remembered to a different degree than when). We tested this hypothesis by training hummingbirds to a memory task, where the location of a reward was specified according to colour (what), location (where), and order and time of day (when). Although hummingbirds remembered these three pieces of information together more often than expected, there was a hierarchy as to how they were remembered. When seemed to be the hardest to remember, while errors relating to what were more easily corrected. Furthermore, when appears to have been encoded as a combination of time of day and sequence information. As hummingbirds solved this task using reconstruction of different memory components (what, where and when), we suggest that similar deconstructive approaches may offer a useful way to compare episodic and episodic-like memories.