Learning the ecological niche

A cornerstone of ecological theory is the ecological niche. Yet little is known about how individuals come to adopt it: whether it is innate or learned. Here, we report a cross-fostering experiment in the wild where we transferred eggs of blue tits, Cyanistes caeruleus, to nests of great tits, Parus major, and vice versa, to quantify the consequences of being reared in a different social context, but in an environment otherwise natural to the birds. We show that early learning causes a shift in the feeding niche in the direction of the foster species and that this shift lasts for life (foraging conservatism). Both species changed their feeding niches, but the change was greater in the great tit with its less specialized feeding behaviour. The study shows that cultural transmission through early learning is fundamental to the realization of ecological niches, and suggests a mechanism to explain learned habitat preference and sympatric speciation in animals.     

Foraging Trade‐offs between Prey Size,Delivery Rate and Prey Type: How Does Niche Breadth and Early Learning of the Foraging Niche Affect Food Delivery?

Optimal foraging theory suggests that avian parents should prefer the most energetically efficient (largest) prey items when delivering food to offspring at a central place. However, during periods of high demand, selectivity of prey may decline, leading to the delivery of smaller and/or less nutritious items. We compared foraging trade‐offs between great tits (Parus major) which had a wider feeding niche than blue tits (Cyanistes caeruleus). We also compared the foraging efficiency of cross‐fostered young, which had learned the spatial foraging niche and prey size of the foreign species, to that of control conspecifics. Mean delivery rates did not differ between control and cross‐fostered parents of either species but as delivery rates increased, prey size declined for both species and both treatment groups. However, across the range of increasing delivery rates, parents were able to increase the total biomass of prey delivered. Cross‐fostering did not alter the proportion of different prey taxa in the diet, but cross‐fostered birds shifted the size of the prey taken to that of their foster species. Consistent with their broader feeding niche, great tits, but not blue tits, incorporated more unpalatable items (flies) as delivery rates increased. Although great tits foraged less efficiently in the blue tit niche, paradoxically, blue tits seem to deliver more prey biomass when foraging in the great tit niche.     

Difficulties when assessing birdsong learning programmes under field conditions: a re-evaluation of song repertoire flexibility in the great tit

There is a remarkable diversity of song-learning strategies in songbirds. Establishing whether a species is closed- or open-ended is important to be able to interpret functional and evolutionary consequences of variation in repertoire size. Most of our knowledge regarding the timing of vocal learning is based on laboratory studies, despite the fact that these may not always replicate the complex ecological and social interactions experienced by birds in the wild. Given that field studies cannot provide the experimental control of laboratory studies, it may not be surprising that species such as the great tit that were initially assumed to be closed-ended learners have later been suggested to be open-ended learners. By using an established colour-ringed population, by following a standardized recording protocol, and by taking into account the species' song ecology (using only recordings obtained during peak of singing at dawn), we replicated two previous studies to assess song repertoire learning and flexibility in adult wild great tits elicited by social interactions. First, we performed a playback experiment to test repertoire plasticity elicited by novel versus own songs. Additionally, in a longitudinal study, we followed 30 males in two consecutive years and analysed whether new neighbours influenced any change in the repertoire. Contrary to the previous studies, song repertoire size and composition were found to be highly repeatable both between years and after confrontation with a novel song. Our results suggest that great tits are closed-ended learners and that their song repertoire probably does not change during adulthood. Methodological differences that may have led to an underestimation of the repertoires or population differences may explain the discrepancy in results with previous studies. We argue that a rigorous and standardized assessment of the repertoire is essential when studying age- or playback-induced changes in repertoire size and composition under field conditions.     

Wild‐caught great tits Parus major fail to use tools in a laboratory experiment,despite facilitation

Studies investigating tool use in animals that are not known tool users in the wild are important in helping to understand how and under what circumstances this ability might arise. Tool use appears to be uncommon in great tits (Parus major), with only a single documented observation in which a wild great tit used conifer needles to extract larvae from crevices in trees. In a laboratory‐based experiment, we examined whether wild‐caught great tits could learn to use tools in a similar manner. We presented the birds with two different tool use tasks in which they would need to use either a stick or a hook to extract an otherwise inaccessible meal worm from a transparent plastic tube. First, the birds passed a simpler training criterion (pulling a tool with an attached food reward) that aimed to reduce the difficulty of the task. Nevertheless, none of the individuals learnt to use tools in either of the two tasks. This result stands in stark contrast to the abilities of some corvids and parrots, which can learn to use tools in captivity, even though some of them are not tool users in the wild. We believe that tool use might be difficult for some birds to learn since the skills required for this ability seem not to be part of their natural foraging behaviour.     

Effects of experimental night lighting on the daily timing of winter foraging in common European songbirds

The ecological effects of light pollution are becoming better understood, especially in birds. Recent studies have shown that several bird species can use street lighting to extend activity into the night during the breeding season. However, most of these studies are correlational and little is known about the effects of artificial night lighting on the timing of activities outside the breeding season. During winter, low temperatures and short days may limit foraging opportunities and can negatively affect survival of resident birds. However, night lighting may allow them to expand the time niche available for foraging. Here, we report on a study where we repeatedly manipulated the amount of night lighting during early winter at automated feeding stations in a natural forest. We used video‐recordings at the feeders to determine the time of the first (at dawn) and last (at dusk) foraging visits for six songbird species. We predicted that all species, and in particular the naturally early‐foraging species, would advance their daily onset of foraging during the mornings with night lighting, but would show minimal or no delays in their daily cessation of foraging during the lighted evenings. We found that two early‐foraging species, the blue tit and the great tit, started foraging earlier during the experimentally lighted mornings. However, in great tits, this effect was weak and restricted to nights with inclement weather. The light treatment did not have any effect on the start of foraging in the willow/marsh tit, the nuthatch, the European jay, and the blackbird. Artificial night lighting did not cause later foraging at dusk in any of the six species. Overall, our results suggest that artificial light during winter has only small effects on timing of foraging. We discuss these findings and the importance of temperature and winter weather in shaping the observed foraging patterns.     

Does foraging behaviour explain the poor breeding success of great tits Parus major in northern Europe?

Great tits Parus major have generally much poorer breeding success in northern Finland than in mid- and western Europe. The aim of this study is to find out whether the poor success is linked to foraging behaviour. This was studied by monitoring great tits' foraging behaviour and food abundance in different substrates during the breeding cycle in two populations, N Finland (65°N) and Latvia (56°N). It was shown that breeding success, from eggs to fledglings, was significantly poorer (56% vs. 93%) and caterpillar abundance considerably lower in the northern population. The general patterns in foraging behaviour were the same in N Finland and Latvia (especially the preference of birches Betula spp.) indicating that great tits used basically the same species-typical foraging strategy in both populations. However, thin branches of birch were preferred in the north but avoided in Latvia, which may suggest that northern great tits have changed their foraging niche towards the outer parts of canopy, a niche typically occupied by the blue tit. This shift is theoretically advantageous, since the outer parts of the canopy are the richest caterpillar source. In practice, however, the poorer success of great tits indicates that this is not a beneficial strategy. Primarily, great tits in the northern population seem to be food limited since they lay too large clutches in relation to accessible food resources. This may be because great tits are not adapted to lower caterpillar production in the northern margins of their distribution and cannot change their narrow diet (3/4 caterpillars), like e.g. willow tits can. In search for caterpillars, food accessibility is further limited because the great tits' normal foraging behaviour, with wide search radius, may not function properly in the denser, outer parts of the canopy. Great tits may also be too heavy to forage efficiently on leafed twigs.     

Fat reserves and perceived predation risk in the great tit, Parus major

The fat reserves of small birds are built up daily as insurance against starvation. They are believed to reflect a trade-off between the risks of starvation and predation such that in situations of high predation risk birds are expected either to reduce their fat reserves in response to mass-dependent predation risk or to increase them in response to foraging interruptions. We assessed the effect on fat reserves of experimentally altering the perceived (but not the actual) risk of predation of wild great tits at a winter feeding site. The perceived predation risk was alternated between 'safe' and 'risky'. Increasing the perceived risk of predation involved 'swooping' a model sparrowhawk over the feeder at four unpredictable times each day using a remote mechanism We produce evidence that the experiment was suceessfull in altering the perceived risk of predation. As predicted from the hypothesis of mass-dependent predation risk, great tits (Parus major) carried significantly reduced fat reserves during the 'risky' treatment. Furthermore, dominant individuals were able to reduce their reserves more than subordinates. As birds returned to feeders within seconds after a predator 'attack', the reduction in fat reserves cannot be attributed to an interruption in feeding.     

Task‐Dependent Differences in Learning by Subordinate and Dominant Wild Arabian Babblers

Learning and innovation abilities have been studied extensively in flocking birds, but their importance and relevance in cooperatively breeding birds have been relatively unexplored. We studied the acquisition of novel foraging skills in 14 groups of wild, cooperatively breeding Arabian babblers (Turdoides squamiceps). While in a previous study we found that subordinate individuals were usually the first to learn to remove black rubber lids from a foraging grid, here we show that dominant individuals were the first to succeed in shifting from these black rubber lids to newly introduced white rubber lids. We also found that in all groups where one forager learned to shift to the white lids, the rest of the foragers also learned to do so, suggesting that this behaviour may be transmitted among group members. Although dominant individuals were almost always the first to remove white lids, once starting to remove white lids, dominants and subordinates learned equally well to prefer white over black lids based on differential reinforcement (food was provided only under white lids). Together with our previous study, our results suggest that differences in learning between dominants and subordinates may be task‐specific, which may represent different cognitive strategies: subordinates may explore a more diverse range of foraging opportunities, while dominants may be better at generalizing from familiar tasks to similar ones.     

Reduced dietary conservatism in a wild bird in the presence of intraspecific competition

The presence of intraspecific competitors can increase foraging costs through exploitation of resources. Optimal foraging theory suggests that when the cost of pursuing one food type increases, alternative resources should be accepted. Accepting novel foods readily might put a competitor at an advantage over its more conservative rivals in the race for sufficient sustenance, but also opens it to the danger of poisoning by chemically protected food. Dietary conservatism is a foraging behaviour characterised by a prolonged avoidance of novel foods, long after neophobia (initial fear of novel objects) has been overcome, and so might be seen as a disadvantage to foragers in a competitive situation. There are two stable foraging strategies found within forager populations: 1) adventurous consumers (AC) which rapidly accept novel foods and 2) foragers showing dietary conservatism (DC). The expression of these two strategies may also vary with environmental conditions. The aim of this study was to investigate the effect of intraspecific competition on the levels of dietary conservatism displayed among wild caught blue tits Cyanistes caeruleus. Blue tits were offered items of both novel and familiar foods under two conditions: with a competitor and without. Our results showed that individuals who experienced competition incorporated the novel items into their diet faster than those who did not experience competition. This study demonstrates, for the first time, the degree of plasticity in the expression of the DC trait using wild birds in laboratory conditions. This plasticity represents a significant adaptation to reduce the costs of foraging conservatively when novel alternative resources should be accepted.     

Sexual imprinting and the origin of obligate brood parasitism in birds

We discuss two pathways along which obligate brood parasitism (OBP) may evolve and examine some of the critical steps that must be passed by letting great tits Parus major be reared by blue tits Parus caeruleus in a field experiment. The cross-fostered chicks survived well in blue tit nests, but their local recruitment and reproductive success was much lower than that of controls. The effect was strongest when great tits grew up with siblings of the host species rather than with conspecific siblings in blue tit nests. The low success seemed to be caused by misimprinting because the cross-fostered birds behaved like blue tits in several aspects (species association, alarm calls, and aggressive response by resident females to caged intruders). Some birds of both sexes were apparently so strongly imprinted that they did not attract or accept a social mate of their own species. We conclude that imprinting may be necessary for OBP to evolve in birds because the parasite must be attracted to the nests of the host species to add eggs and thereby continue the parasitic life cycle. However, strong imprinting may also prevent OBP from occurring if parasitic offspring seek a mate from the host species.     

Foraging Behaviour of Subordinate Great Tits (Parus major). Can Morphology Reduce the Cost of Subordination?

This paper studies the magnitude of the behavioural shift, from forage standing to forage hanging, of subordinate great tits ( Parus major ) in two different social contexts: feeding solitarily vs. feeding with a dominant conspecific. The aim is to test the hypothesis that differences in morphological design provide subordinates with varying abilities to reduce the presumed costs of subordination. We find that different subordinate individuals change the foraging behaviour, occupying a different niche when an intra-specific competitor is present. Morphology linked to sexual dimorphism, specifically body mass, is the factor responsible for the different magnitudes of change. Lighter subordinates can remain longer than heavier ones at the feeding patch without interrupting their foraging. Thereby, the former reduce the costs of being subordinate more than the latter. Among subordinates, females are lighter than males; they also spend more time feeding in the presence of a dominant conspecific than males do. No differences are found between age categories. We find no relationship between tarsus length and individual ecological plasticity. Our results support the idea that the ecological plasticity due to morphological differences is a mechanism that allows subordinate individuals to overcome costs associated with subordination.     

Activity patterns during food provisioning are affected by artificial light in free living great tits (Parus major)

Artificial light may have severe ecological consequences but there is limited experimental work to assess these consequences. We carried out an experimental study on a wild population of great tits (Parus major) to assess the impact of light pollution on daily activity patterns during the chick provisioning period. Pairs that were provided with a small light outside their nest box did not alter the onset, cessation or duration of their working day. There was however a clear effect of artificial light on the feeding rate in the second half of the nestling period: when provided with artificial light females increased their feeding rate when the nestlings were between 9 and 16 days old. Artificial light is hypothesised to have affected the perceived photoperiod of either the parents or the offspring which in turn led to increased parental care. This may have negative fitness consequences for the parents, and light pollution may thus create an ecological trap for breeding birds.     

Identification of learning mechanisms in a wild meerkat population

Vigorous debates as to the evolutionary origins of culture remain unresolved due to an absence of methods for identifying learning mechanisms in natural populations. While laboratory experiments on captive animals have revealed evidence for a number of mechanisms, these may not necessarily reflect the processes typically operating in nature. We developed a novel method that allows social and asocial learning mechanisms to be determined in animal groups from the patterns of interaction with, and solving of, a task. We deployed it to analyse learning in groups of wild meerkats (Suricata suricatta) presented with a novel foraging apparatus. We identify nine separate learning processes underlying the meerkats' foraging behaviour, in each case precisely quantifying their strength and duration, including local enhancement, emulation, and a hitherto unrecognized form of social learning, which we term 'observational perseverance'. Our analysis suggests a key factor underlying the stability of behavioural traditions is a high ratio of specific to generalized social learning effects. The approach has widespread potential as an ecologically valid tool to investigate learning mechanisms in natural groups of animals, including humans.     

Great tits do not compensate over time for a radio‐tag‐induced reduction in escape‐flight performance

The use of biologging and tracking devices is widespread in avian behavioral and ecological studies. Carrying these devices rarely has major behavioral or fitness effects in the wild, yet it may still impact animals in more subtle ways, such as during high power demanding escape maneuvers. Here, we tested whether or not great tits (Parus major) carrying a backpack radio‐tag changed their body mass or flight behavior over time to compensate for the detrimental effect of carrying a tag. We tested 18 great tits, randomly assigned to a control (untagged) or one of two different types of a radio‐tag as used in previous studies in the wild (0.9 g or 1.2 g; ~5% or ~6–7% of body mass, respectively), and determined their upward escape‐flight performance 1, 7, 14, and 28 days after tagging. In between experiments, birds were housed in large free‐flight aviaries. For each escape‐flight, we used high‐speed 3D videography to determine flight paths, escape‐flight speed, wingbeat frequency, and actuator disk loading (ratio between the bird weight and aerodynamic thrust production capacity). Tagged birds flew upward with lower escape‐flight speeds, caused by an increased actuator disk loading. During the 28‐day period, all groups slightly increased their body mass and their in‐flight wingbeat frequency. In addition, during this period, all groups of birds increased their escape‐flight speed, but tagged birds did so at a lower rate than untagged birds. This suggests that birds may increase their escape‐flight performance through skill learning; however, tagged birds still remained slower than controls. Our findings suggest that tagging a songbird can have a prolonged effect on the performance of rapid flight maneuvers. Given the absence of tag effects on reproduction and survival in most songbird radio‐tagging studies, tagged birds in the wild might adjust their risk‐taking behavior to avoid performing rapid flight maneuvers.     

Ultraviolet cues affect the foraging behaviour of blue tits

The function of avian ultraviolet (UV) vision is only just beginning to be understood. One plausible hypothesis is that UV vision enhances the foraging ability of birds. To test this, we carried out behavioural experiments using wild-caught blue tits foraging for cabbage moth and winter moth caterpillars on natural and artificial backgrounds. The light environment in our experiments was manipulated using either UV-blocking or UV-transmitting filters. We found that the blue tits tended to find the first prey item (out of four) more quickly when UV cues were present. This suggests that UV vision offers benefits to birds when searching for cryptic prey, despite the prey and backgrounds reflecting relatively little UV. Although there was no direct effect of UV on the time taken to find all four prey items in a trial, search performance in the absence of UV wavelengths tended to increase over the course of an experiment. This may reflect changes in the search tactics of the birds. To our knowledge, these are the first data to suggest that birds use UV cues to detect cryptic insect prey, and have implications for our understanding of protective coloration.     

Effect of Daily Body Mass Variation on the Foraging Behaviour of Tit Species (Parus spp.)

We studied the effect of daily body mass increase on the foraging preferences of two tit species, crested tit, Parus cristatus and blue tit, P. caeruleus, contrasting in morphology and behaviour. We found that both species show a diurnal increase in body mass during winter. Using an experiment with feeders we show that in the crested tit, the proportion of time spent foraging while hanging decreased as body mass increased. In contrast, in the blue tit, foraging behaviour did not change with mass gain. We propose that the species with a morphological design providing a high ecological plasticity in terms of foraging postures can counteract the negative effect of body mass on the ecological options (foraging niche) more than species with a morphological design providing a low ecological plasticity in terms of foraging postures. Our results suggest that blue tits had the advantage of being able to choose to feed on different patches in the habitat throughout the day, which makes resources more predictable for them. In contrast, crested tits might be more restricted in their foraging options as their body mass increases, and this might explain why they hoard food.     

Linking individual foraging behavior and population spatial distribution in patchy environments: a field example with Mediterranean blue tits

 In spite of recent theoretical interest, few field studies have addressed the links between individual behavioral decisions and population distribution. This work analyzes the foraging behavior of individuals and the spatial distribution of a population of blue tits (Parus caeruleus) just before the main breeding season, when blue tit foraging was not affected by central-place or flocking behaviors. The study was carried out in open holm oak Quercus ilex woodlands (dehesas) that are patchy for canopy-foraging birds because of the scattered arrangement of trees. Residence time on each tree was not correlated either with previous flight time or with prey abundance in trees. Flight distances between trees were larger than average distances estimated in random samples of holm oaks taken close to foraging birds. Trees were not selected by birds on the basis of their expected energy costs and rewards. Bird abundance was not related to food availability in trees or to tree size across dehesas. However, bird abundance was strongly correlated with tree density and with the availability of tree holes for nesting, to the extent that the proportion of tits matched the proportions of both tree abundance and hole abundance across study plots. Overall, neither the behavior of individuals nor the distribution of the population of blue tits corresponded with food resources, which appeared superabundant; instead, tits appeared to behave and be distributed according to the distribution of structural resources such as trees and tree holes for nesting. Received: 18 August 1996 / Accepted: 14 March 1997     

Scrounging Tactics in Free-Ranging Ravens, Corvus corax

Social foraging allows individuals to scrounge, i.e. to exploit the food others have made available. The conditions promoting scrounging as an alternative foraging tactic have yet received limited attention. We presently examine whether ravens, as opportunistic scavengers, adjust their foraging tactics according to the potential costs involved in accessing a particular food source. We observed wild ravens foraging in a game park, at the enclosures of wolves, Canis lupus, and wild boars, Sus scrofa. Wolves may aggressively defend their food and even kill ravens, whereas wild boars do not. When co‐feeding with wolves, the ravens showed higher scrounging rates than with wild boars. Only at the wolves, they tended to specialize either on scrounging or on getting food directly from the site. However, scrounging techniques differed in relation to the state of food depletion. Early on, after food became available, the ravens most frequently displaced others from food, whereas towards the end, stealing, solicited sharing, and cache raiding became prevalent. These techniques differed in their profitability and their use was related to the scroungers’ age, social status and affiliative relationships. This suggests that ecological conditions, such as co‐feeding with potential predators, may influence the individuals’ decision whether or not to scrounge in competition for food. Social conditions, on the other hand, may affect the way how to get at food possessed by others and may thus, to a large extent, determine the profitability of scrounging.     

Does predation maintain tit community diversity?

European tits of the genus Parus constitute a complex group of coexisting boreal birds. Here we present a survey of the distribution of three coniferous-living Parus species and one of their main predators, the pygmy owl ( Glaucidium passerinum ), on nine isolated islands in Scandinavia. On all islands the coal tit ( Parus ater ) is the sole tit species when the pygmy owl is absent. The two larger species, the willow tit ( P. montanus ) and the crested tit ( P. cristatus ), only coexist with the coal tit when pygmy owls are present. We suggest that the coexistence of willow tits, crested tits and coal tits is the result of a combination of competition for food and predator-safe foraging sites. The smaller coal tit is superior in exploitation competition for food, while the two larger species have an advantage in interference competition for predator-safe foraging sites. The association between the distribution of the pygmy owl and the two larger tit species on isolated islands in Scandinavia is consistent with the idea that the pygmy owl is a keystone predator.     

Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring

Early nutrition shapes life history. Parents should, therefore, provide a diet that will optimize the nutrient intake of their offspring. In a number of passerines, there is an often observed, but unexplained, peak in spider provisioning during chick development. We show that the proportion of spiders in the diet of nestling blue tits, Cyanistes caeruleus, varies significantly with the age of chicks but is unrelated to the timing of breeding or spider availability. Moreover, this parental prey selection supplies nestlings with high levels of taurine particularly at younger ages. This amino acid is known to be both vital and limiting for mammalian development and consequently found in high concentrations in placenta and milk. Based on the known roles of taurine in mammalian brain development and function, we then asked whether by supplying taurine-rich spiders, avian parents influence the stress responsiveness and cognitive function of their offspring. To test this, we provided wild blue tit nestlings with either a taurine supplement or control treatment once daily from the ages of 2-14 days. Then pairs of size- and sex-matched siblings were brought into captivity for behavioural testing. We found that juveniles that had received additional taurine as neonates took significantly greater risks when investigating novel objects than controls. Taurine birds were also more successful at a spatial learning task than controls. Additionally, those individuals that succeeded at a spatial learning task had shown intermediate levels of risk taking. Non-learners were generally very risk-averse controls. Early diet therefore has downstream impacts on behavioural characteristics that could affect fitness via foraging and competitive performance. Fine-scale prey selection is a mechanism by which parents can manipulate the behavioural phenotype of offspring.