Are comparable studies really comparable? Suggestions from a problem-solving experiment on urban and rural great tits.

Performance in tests of various cognitive abilities has often been compared, both within and between species. In intraspecific comparisons, habitat effects on cognition has been a popular topic, frequently with an underlying assumption that urban animals should perform better than their rural conspecifics. In this study, we tested problem-solving ability in great tits Parus major, in a string-pulling and a plug-opening test. Our aim was to compare performance between urban and rural great tits, and to compare their performance with previously published problem solving studies. Our great tits perfomed better in string-pulling than their conspecifics in previous studies (solving success: 54%), and better than their close relative, the mountain chickadee Poecile gambeli, in the plug-opening test (solving success: 70%). Solving latency became shorter over four repeated sessions, indicating learning abilities, and showed among-individual correlation between the two tests. However, the solving ability did not differ between habitat types in either test. Somewhat unexpectedly, we found marked differences between study years even though we tried to keep conditions identical. These were probably due to small changes to the experimental protocol between years, for example the unavoidable changes of observers and changes in the size and material of test devices. This has an important implication: if small changes in an otherwise identical set-up can have strong effects, meaningful comparisons of cognitive performance between different labs must be extremely hard. In a wider perspective this highlights the replicability problem often present in animal behaviour studies.

Feather corticosterone reveals that urban great tits experience lower corticosterone exposure than forest individuals during dominance-rank establishment.

Although the consequences of urbanization for the physiological health of animals are the focus of much active research, an overlooked aspect is how physiology could be indirectly modulated by the urban environment via changes in intraspecific behavioural interactions, particularly among gregarious species. Both urbanization and the establishment, as well as maintenance, of hierarchical rank position are processes that could incur physiological stress. Measurements of glucocorticoids (GCs) in relation to urbanization, however, have yielded inconsistent results. In most cases, GCs have been measured in blood, offering only a 'snapshot' of an animal's current physiological state. Because circulating GCs are incorporated into growing feathers or hair, measurements of feather/hair GCs offer a longer term measure of stress exposure reflecting the whole period of feather/hair growth. During two calendar years, we collected tail feathers from 188 urban and forest great tits (P. major) across multiple sampling sites and analysed corticosterone (CORT-the main GC in birds) levels, reflecting CORT exposure during the extended period in late summer and early autumn when great tits moult and winter flocks are formed. Urban individuals exhibited consistently lower feather CORT (fCORT) levels than forest birds indicating lower overall exposure to CORT during this period. The lower fCORT levels in urban individuals could represent an adaptation to cope with the more challenging urban environment, physiological constraints on stress axis function or a trade-off between the ability to respond to stressors and predation risk during moult. Despite the expectation that CORT responses to urbanization are highly context-dependent, the spatial consistency of our results and agreement with a multi-population study of fCORT in European blackbirds (Turdus merula) suggests a generalization of the effect of urbanization on CORT exposure during post-breeding moult (i.e. not site- or species-specific).

Blue tits are outperformed by great tits in a test of motor inhibition, and experience does not improve their performance.

Motor inhibition refers to the ability to inhibit immediate responses in favour of adaptive actions that are mediated by executive functions. This ability may be an indication of general cognitive ability in animals and is important for advanced cognitive functions. In this study, our aim was to compare motor inhibition ability of two closely related passerines that share the same habitat. To do this, we tested motor inhibition ability using a transparent cylinder task in blue tits in the same way as we previously tested great tits. To test whether the experience of transparent objects would affect the performance of these species differently, both in the present experiment using blue tits and our previous one on great tits, we divided 33 wild-caught individuals into three different treatment groups with 11 birds each. Before the test we allowed one group to experience a transparent cylindrical object, one group to experience a transparent wall and a third group was kept naive. In general, blue tits performed worse than great tits, and unlike the great tits, they did not improve their performance after experience with a transparent cylinder-like object. The performance difference may stem from difference in foraging behaviour between these species.

Birds differentially prioritize visual and olfactory foraging cues depending on habitat of origin and sex.

Animals interpret their environment by combining information from multiple senses. The relative usefulness of different senses may vary between species, habitats and sexes; yet, how multimodal stimuli are integrated and prioritized is unknown for most taxa. We experimentally assessed foraging preferences of great tits (Parus major) to test whether urban and forest individuals prioritize visual and olfactory cues differently during foraging. We trained 13 wild-caught birds to associate multimodal (colour + odour) cues with a food reward and assessed their foraging preferences in a cue-separation test. In this, the birds could choose between the multimodal training cue and its olfactory or visual components. Our results suggest that the birds did not perceive multimodal cues in an integrated way, as their response was not stronger than for unimodal cue components. Urban birds preferred olfactory cues, while forest birds preferred visual cues. Nevertheless, female birds preferred the multimodal cue, while males foraged more randomly with respect to which cue was present. These findings contribute to our understanding of the relative roles of vision and olfaction in bird foraging behaviour. Future work should focus on how habitat- and sex-specific sensory prioritization modifies bird foraging behaviour and foraging success in the context of urban adaptations across populations.

High level of self-control ability in a small passerine bird.

ABSTRACT: Cognitively advanced animals are usually assumed to possess better self-control, or ability to decline immediate rewards in favour of delayed ones, than less cognitively advanced animals. It has been claimed that the best predictor of high such ability is absolute brain volume meaning that large-brained animals should perform better than small-brained ones. We tested self-control ability in the great tit, a small passerine. In the common test of this ability, the animal is presented with a transparent cylinder that contains a piece of food. If the animal tries to take the reward through the transparent wall of the cylinder, this is considered an impulsive act and it fails the test. If it moves to an opening and takes the reward this way, it passes the test. The average performance of our great tits was 80%, higher than most animals that have been tested and almost in level with the performance in corvids and apes. This is remarkable considering that the brain volume of a great tit is 3% of that of a raven and 0.1% of that of a chimpanzee. SIGNIFICANCE STATEMENT: The transparent cylinder test is the most common way to test the ability of self-control in animals. If an animal understands that it only can take food in the cylinder from the cylinder's opening and controls its impulsivity, it passes the test. A high level of self-control has been demonstrated only in cognitively advanced animals such as apes and corvids. Here, we demonstrate that the great tit, a small song bird that is very good at learning, performs almost in level with chimpanzees and ravens in this test.

Adaptive temperature regulation in the little bird in winter: predictions from a stochastic dynamic programming model.

Several species of small birds are resident in boreal forests where environmental temperatures can be -20 to -30 °C, or even lower, in winter. As winter days are short, and food is scarce, winter survival is a challenge for small endothermic animals. A bird of this size will have to gain almost 10% of its lean body mass in fat every day to sustain overnight metabolism. Birds such as parids (titmice and chickadees) can use facultative hypothermia, a process in which body temperature is actively down-regulated to a specific level, to reduce heat loss and thus save energy. During cold winter nights, these birds may decrease body temperature from the normal from 42 ° down to 35 °C, or even lower in some species. However, birds are unable to move in this deep hypothermic state, making it a risky strategy if predators are around. Why, then, do small northern birds enter a potentially dangerous physiological state for a relatively small reduction in energy expenditure? We used stochastic dynamic programming to investigate this. Our model suggests that the use of nocturnal hypothermia at night is paramount in these biomes, as it would increase winter survival for a small northern bird by 58% over a winter of 100 days. Our model also explains the phenomenon known as winter fattening, and its relationship to thermoregulation, in northern birds.

No evidence for self-recognition in a small passerine, the great tit (Parus major) judged from the mark/mirror test.

Self-recognition is a trait presumed to be associated with high levels of cognition and something previously considered to be exclusive to humans and possibly apes. The most common test of self-recognition is the mark/mirror test of whether an animal can understand that it sees its own reflection in a mirror. The usual design is that an animal is marked with a colour spot somewhere on the body where the spot can only be seen by the animal by using a mirror. Very few species have passed this test, and among birds, only magpies have been affirmatively demonstrated to pass it. In this study, we tested great tits (Parus major), small passerines, that are known for their innovative foraging skills and good problem-solving abilities, in the mirror self-recognition test. We found no indication that they have any ability of this kind and believe that they are unlikely to be capable of this type of self-recognition.

Evidence against observational spatial memory for cache locations of conspecifics in marsh tits Poecile palustris.

ABSTRACT: Many species in the family Paridae, such as marsh tits Poecile palustris, are large-scale scatter hoarders of food that make cryptic caches and disperse these in large year-round territories. The perhaps most well-known species in the family, the great tit Parus major, does not store food itself but is skilled in stealing caches from the other species. We have previously demonstrated that great tits are able to memorise positions of caches they have observed marsh tits make and later return and steal the food. As great tits are explorative in nature and unusually good learners, it is possible that such "memorisation of caches from a distance" is a unique ability of theirs. The other possibility is that this ability is general in the parid family. Here, we tested marsh tits in the same experimental set-up as where we previously have tested great tits. We allowed caged marsh tits to observe a caching conspecific in a specially designed indoor arena. After a retention interval of 1 or 24 h, we allowed the observer to enter the arena and search for the caches. The marsh tits showed no evidence of such observational memorization ability, and we believe that such ability is more useful for a non-hoarding species. Why should a marsh tit that memorises hundreds of their own caches in the field bother with the difficult task of memorising other individuals' caches? We argue that the close-up memorisation procedure that marsh tits use at their own caches may be a different type of observational learning than memorisation of caches made by others. For example, the latter must be done from a distance and hence may require the ability to adopt an allocentric perspective, i.e. the ability to visualise the cache from the hoarder's perspective. SIGNIFICANCE STATEMENT: Members of the Paridae family are known to possess foraging techniques that are cognitively advanced. Previously, we have demonstrated that a non-hoarding parid species, the great tit P. major, is able to memorise positions of caches that they have observed marsh tits P. palustris make. However, it is unknown whether this cognitively advanced foraging strategy is unique to great tits or if it occurs also in other parids. Here, we demonstrated that "pilfering by observational memorization strategy" is not a general strategy in parids. We believe that such ability is important for a non-hoarding species such as the great tit and, most likely, birds owning many caches do not need this foraging strategy.

No evidence for memory interference across sessions in food hoarding marsh tits Poecile palustris under laboratory conditions.

Scatter hoarding birds are known for their accurate spatial memory. In a previous experiment, we tested the retrieval accuracy in marsh tits in a typical laboratory set-up for this species. We also tested the performance of humans in this experimental set-up. Somewhat unexpectedly, humans performed much better than marsh tits. In the first five attempts, humans relocated almost 90 % of the caches they had hidden 5 h earlier. Marsh tits only relocated 25 % in the first five attempts and just above 40 % in the first ten attempts. Typically, in this type of experiment, the birds will be caching and retrieving many times in the same sites in the same experimental room. This is very different from the conditions in nature where hoarding parids only cache once in a caching site. Hence, it is possible that memories from previous sessions will disturb the formation of new memories. If there is such proactive interference, the prediction is that success should decay over sessions. Here, we have designed an experiment to investigate whether there is such memory interference in this type of experiment. We allowed marsh tits and humans to cache and retrieve in three repeated sessions without prior experience of the arena. The performance did not change over sessions, and on average, marsh tits correctly visited around 25 % of the caches in the first five attempts. The corresponding success in humans was constant across sessions, and it was around 90 % on average. We conclude that the somewhat poor performance of the marsh tits did not depend on proactive memory interference. We also discuss other possible reasons for why marsh tits in general do not perform better in laboratory experiments.

An evaluation of memory accuracy in food hoarding marsh tits Poecile palustris--how accurate are they compared to humans?

Laboratory studies of scatter hoarding birds have become a model system for spatial memory studies. Considering that such birds are known to have a good spatial memory, recovery success in lab studies seems low. In parids (titmice and chickadees) typically ranging between 25 and 60% if five seeds are cached in 50-128 available caching sites. Since these birds store many thousands of food items in nature in one autumn one might expect that they should easily retrieve five seeds in a laboratory where they know the environment with its caching sites in detail. We designed a laboratory set up to be as similar as possible with previous studies and trained wild caught marsh tits Poecile palustris to store and retrieve in this set up. Our results agree closely with earlier studies, of the first ten looks around 40% were correct when the birds had stored five seeds in 100 available sites both 5 and 24h after storing. The cumulative success curve suggests high success during the first 15 looks where after it declines. Humans performed much better, in the first five looks most subjects were 100% correct. We discuss possible reasons for why the birds were not doing better.

A role for learning in population divergence of mate preferences.

Learning and other forms of phenotypic plasticity have been suggested to enhance population divergence. Mate preferences can develop by learning, and species recognition might not be entirely genetic. We present data on female mate preferences of the banded demoiselle (Calopteryx splendens) that suggest a role for learning in population divergence and species recognition. Populations of this species are either allopatric or sympatric with a phenotypically similar congener (C. virgo). These two species differ mainly in the amount of wing melanization in males, and wing patches thus mediate sexual isolation. In sympatry, sexually experienced females discriminate against large melanin wing patches in heterospecific males. In contrast, in allopatric populations within the same geographic region, females show positive ("open-ended") preferences for such large wing patches. Virgin C. splendens females do not discriminate against heterospecific males. Moreover, physical exposure experiments of such virgin females to con- or hetero-specific males significantly influences their subsequent mate preferences. Species recognition is thus not entirely genetic and it is partly influenced by interactions with mates. Learning causes pronounced population divergence in mate preferences between these weakly genetically differentiated populations, and results in a highly divergent pattern of species recognition at a small geographic scale.

The history of scatter hoarding studies.

In this review, I will present an overview of the development of the field of scatter hoarding studies. Scatter hoarding is a conspicuous behaviour and it has been observed by humans for a long time. Apart from an exceptional experimental study already published in 1720, it started with observational field studies of scatter hoarding birds in the 1940s. Driven by a general interest in birds, several ornithologists made large-scale studies of hoarding behaviour in species such as nutcrackers and boreal titmice. Scatter hoarding birds seem to remember caching locations accurately, and it was shown in the 1960s that successful retrieval is dependent on a specific part of the brain, the hippocampus. The study of scatter hoarding, spatial memory and the hippocampus has since then developed into a study system for evolutionary studies of spatial memory. In 1978, a game theoretical paper started the era of modern studies by establishing that a recovery advantage is necessary for individual hoarders for the evolution of a hoarding strategy. The same year, a combined theoretical and empirical study on scatter hoarding squirrels investigated how caches should be spaced out in order to minimize cache loss, a phenomenon sometimes called optimal cache density theory. Since then, the scatter hoarding paradigm has branched into a number of different fields: (i) theoretical and empirical studies of the evolution of hoarding, (ii) field studies with modern sampling methods, (iii) studies of the precise nature of the caching memory, (iv) a variety of studies of caching memory and its relationship to the hippocampus. Scatter hoarding has also been the subject of studies of (v) coevolution between scatter hoarding animals and the plants that are dispersed by these.

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus.

A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.

An analysis of population genetic differentiation and genotype-phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R.

The all black carrion crow (Corvus corone corone) and the grey and black hooded crow (Corvus corone cornix) meet in a narrow hybrid zone across Europe. To evaluate the degree of genetic differentiation over the hybrid zone, we genotyped crows from the centre and edges of the zone, and from allopatric populations in northern (Scotland-Denmark-Sweden) and southern Europe (western-central northern Italy), at 18 microsatellites and at a plumage candidate gene, the MC1R gene. Allopatric and edge populations were significantly differentiated on microsatellites, and populations were isolated by distance over the hybrid zone in Italy. Single-locus analyses showed that one locus, CmeH9, differentiated populations on different sides of the zone at the same time as showing only weak separation of populations on the same side of the zone. Within the hybrid zone there was no differentiation of phenotypes at CmeH9 or at the set of microsatellites, no excess of heterozygotes among hybrids and low levels of linkage disequilibrium between markers. We did not detect any association between phenotypes and nucleotide variation at MC1R, and the two most common haplotypes occurred in very similar frequencies in carrion and hooded crows. That we found a similar degree of genetic differentiation between allopatric and edge populations irrespectively of their location in relation to the hybrid zone, no differentiation between phenotypes within the hybrid zone, and neither heterozygote excess nor consistent linkage disequilibrium in the hybrid zone, is striking considering that carrion and hooded crows are phenotypically distinct and sometimes recognised as separate species.

Factors influencing route choice by avian migrants: a dynamic programming model of Pacific brant migration.

We used stochastic dynamic programming to investigate a spectacular migration strategy in the black brant Branta bernicla nigricans, a species of goose. Black brant migration is well suited for theoretical analysis since there are a number of existing strategies that easily can be compared. In early autumn, almost the entire population of the black brant gathers at Izembek Lagoon on the Alaska Peninsula to stage and refuel before the southward migration. There are at least three distinct strategies, with most geese making a spectacular direct migration more than 5000km across the Gulf of Alaska to their wintering grounds in southern Baja California or mainland Mexico. This is a potentially dangerous strategy since foraging is not possible during the overseas passage. Some individuals instead use shorter flights to make a detour along the coast, a longer route that all individuals use for northwards migration in spring. Since flight costs accelerate with increasing body mass, migration by short flights is energetically cheaper than long-distance flights. A small but increasing part of the population has recently begun to winter at Izembek. We investigated this migration under two different suppositions using a dynamic state variable model. First, if the geese are free to make a strategic choice, under what assumptions should they prefer direct migration and under what assumptions should they prefer detour migration/winter residency? Second, provided that the dominating direct migration strategy is optimal, what conditions will force the geese to go for detour migration/winter residency? In the second case the geese may try to follow an optimal direct migration strategy, but stochastic events may force them to choose a suboptimal policy. We also simulated possible effects of global warming. The model suggests that the fuel level at arrival in Izembek and fuel gain rates are key factors and that tail winds must have been reliable in the past, otherwise direct migration could not have evolved. It also suggests that a change to milder winters may promote an unexpectedly abrupt change from long-distance to short-distance migration or winter residency. Finally, it produced a number of predictions that might be testable in the field.

Theoretical models of adaptive energy management in small wintering birds.

Many small passerines are resident in forests with very cold winters. Considering their size and the adverse conditions, this is a remarkable feat that requires optimal energy management in several respects, for example regulation of body fat reserves, food hoarding and night-time hypothermia. Besides their beneficial effect on survival, these behaviours also entail various costs. The scenario is complex with many potentially important factors, and this has made 'the little bird in winter' a popular topic for theoretic modellers. Many predictions could have been made intuitively, but models have been especially important when many factors interact. Predictions that hardly could have been made without models include: (i) the minimum mortality occurs at the fat level where the marginal values of starvation risk and predation risk are equal; (ii) starvation risk may also decrease when food requirement increases; (iii) mortality from starvation may correlate positively with fat reserves; (iv) the existence of food stores can increase fitness substantially even if the food is not eaten; (v) environmental changes may induce increases or decreases in the level of reserves depending on whether changes are temporary or permanent; and (vi) hoarding can also evolve under seemingly group-selectionistic conditions.

Does hippocampal size correlate with the degree of caching specialization?

A correlation between the degree of specialization for food hoarding and the volume of the hippocampal formation in passerine birds has been accepted for over a decade. The relationship was first demonstrated in family-level comparisons, and subsequently in species comparisons within two families containing a large number of hoarding species, the Corvidae and the Paridae. Recently, this approach has been criticized as invalid and excessively adaptationist. A recent test of the predicted trends with data pooled from previous studies found no evidence for such a correlation in either of these two families. This result has been interpreted as support for the critique. Here we reanalyse the original dataset and also include additional new data on several parid species. Our results show a surprising difference between continents, with North American species possessing significantly smaller hippocampi than Eurasian ones. Controlling for the continent effect makes the hoarding capacity/hippocampal formation correlation clearly significant in both families. We discuss possible reasons for the continent effect.

Is hippocampal volume affected by specialization for food hoarding in birds?

The hypothesis that spatial-memory specialization affects the size of the hippocampus has become widely accepted among scientists. The hypothesis comes from studies on birds primarily in two families, the Paridae (tits, titmice and chickadees) and the Corvidae (crows, nutcrackers, jays, etc.). Many species in these families store food and rely on spatial memory to relocate the cached items. The hippocampus is a brain structure that is thought to be important for memory. Several studies report that hoarding species in these families possess larger hippocampi than non-hoarding relatives, and that species classified as large-scale hoarders have larger hippocampi than less specialized hoarders. We have investigated the largest dataset on hippocampus size and food-hoarding behaviour in these families so far but did not find a significant correlation between food-hoarding specialization and hippocampal volume. The occurrence of such an effect in earlier studies may depend on differences in the estimation of hippocampal volumes or difficulties in categorizing the degree of specialization for hoarding or both. To control for discrepancies in measurement methods we made our own estimates of hippocampal volumes in 16 individuals of four species that have been included in previous studies. Our estimates agreed closely with previous ones, suggesting that measurement methods are sufficiently consistent. Instead, the main reasons that previous studies have found an effect where we did not are difficulties in assessing the degree of hoarding specialization and the fact that smaller subsets of species were compared than in our study. Our results show that a correlation between food-hoarding specialization and hippocampal volume cannot be claimed on the basis of present data in these families.