Comparative studies of cognitive abilities in the Paridae : Evidence from laboratory studies

The Paridae (tits, titmice and chickadees) is a bird family consisting of both food hoarding and non-hoarding species. Many studies have been conducted on birds that are considered to be cognitively advanced, such as parrots and corvids, whereas much less is known about these small passerines. In this thesis, I have investigated the cognitive abilities of two members of the Paridae family; marsh tits and great tits. There is a clear dichotomy in wintering strategy across Paridae, with these two species representing either side. Marsh tits are scatter hoarders that cryptically cache food over large areas, whereas great tits are a non-hoarding generalist species that are known to be particularly behaviourally innovative. First, I tested the spatial memory of marsh tits in a laboratory specifically designed for food hoarding studies. In nature, spatial memory is essential for scatter food hoarders to retrieve cached food. Marsh tits displayed around 40% retrieval success after 10 retrieval attempts. These results were in accordance with the previous food hoarding studies conducted on captive marsh tits. I also tested humans in the same task and found they performed much better than marsh tits as after just five attempts they retrieved 80% of the hidden food. Since marsh tits have specialised spatial memory, one may have expected them to outperform humans. The fact that this was not the case, led us to consider whether the marsh tits were affected by proactive memory interference, whereby more recent memories deteriorate as a result of repeated testing. However, this was not the case, as marsh tits performed similarly in all repetitions of the test. Next, I turned my focus to great tits. It is likely to be advantageous for great tits to have access to food caches created by food hoarders during cold winter months. I investigated whether great tits are capable of memorising the locations of caches created by marsh tits. Great tits were allowed to observe marsh tits while they were hiding food items. They successfully memorised the location of caches made by marsh tits after one hour and 24 hours retention intervals. Although it is remarkable that great tits can memorise caches made by marsh tits, we do not know if this ability is found in other Paridae species. In paper IV, I therefore tested the observational spatial memorisation ability of marsh tits in the same experimental setup. Marsh tits were unable to retrieve the caches they observed being stored by other marsh tits. This implies that they do not use this strategy for foraging and that this ability is not common to all Paridae species.In the Paridae family, sex differences are most pronounced in great tits with clear differences in behaviour, morphology and social hierarchy. Hence, I investigated sex differences in cognition in great tits. In chapter V, I investigated whether males and females displayed differences in cognitive abilities using the observational spatial memory task. Female great tits out performed males in this task. In paper VI, I tested for sex differences in the motor self-regulation ability of great tits using the transparent cylinder task. In this task, a food reward is placed inside a transparent cylinder with openings at both ends. The animal must therefore inhibit its urge to reach directly for the visible food and instead take a detour to one of the open end of the cylinder. In addition, I separated the birds into two groups; one with experience of the cylinder and another with no prior experience. Cylinder-experienced birds had a similar transparent cylinder in their cage for three days prior to the experiment whereas cylinder-naïve birds first encountered the transparent cylinder during the test. Great tits were generally successful at this task. I found no overall sex difference in motor self-regulation ability, however the number of repeats that was required to master the task differed between females and males. Males quickly mastered the task, even with no prior experience. However, males with prior experience did not outperform naïve males. Although females took longer to learn the task, those with prior experience outperformed naïve females. In conclusion, I found cognitive differences between two species that differ in their foraging strategies within the same taxonomic family. I propose that these differences have developed due to the distinct winter foraging strategies of these species. I also found evidence of cognitive sex differences in great tits, which I suggest are the result of sex differences in social hierarchy

Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don't have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities

Interspecific observational memory in a non-caching Parus species, the great tit Parus major

Scatter-hoarding passerine birds have become a model system for research on spatial memory capacity. This research has focussed on two families, the Corvidae (crows, jays, nutcrackers, etc.) and the Paridae (titmice and chickadees). Corvids are considered to have highly developed cognitive skills that sometimes have been compared with the great apes. Even though pilfering, or stealing of caches made by others, is common among scatter-hoarding birds, the ability to memorize positions of caches made by others has only been demonstrated in some species of corvids. In parids, the ability to memorize positions of caches made by others has not been demonstrated. In a laboratory experiment, we allowed caged great tits to observe caching marsh tits and found that they remembered caching locations both 1 and 24 h after observation. This is the first time observational spatial learning of this type explicitly has been demonstrated in a parid. This ability is surprising since the great tit is not itself a food hoarder, meaning that it may not have the special memory adaptations in the brain that specialized food hoarders possess. Also, the memorization process in an observing pilferer may differ from the memorization that hoarders make of own caches. For example, the typical close inspection of the cache that hoarding parids do after caching will usually not be possible from a distance. Also, the visual perspective of the observing scrounger may be different from that of the hoarder, meaning that some understanding of allocentric space may be required

Sex differences in learning ability in a common songbird, the great tit-females are better observational learners than males

In mammals, including humans, the most consistent cognitive sex difference appears to be a male advantage in spatial ability. Usually, some sex-correlated selective advantage is inferred to explain this, for example, the need for males to navigate over large territories. In birds, sex differences in learning abilities are rare. Here, we show that females of a common European songbird, the great tit, do clearly better than males in an observational memorization task. We allowed caged great tits to observe food-caching marsh tits in an indoor aviary. One hour later, the great tits were released to search for the cached food. Females consistently performed better than males in this task. The results are remarkable for several reasons: (i) a sex difference in a cognitive ability of such a magnitude is unusual; (ii) most sex differences in spatial ability that have been reported so far concerns a male advantage; and perhaps most remarkably, (iii) female great tits were as successful in relocating the cached food as the hoarding marsh tits themselves. We hypothesize that female great tits are better at this than males because they are subordinate foragers. Males have prior access to food in nature and can easily displace females. Females will then benefit from a special ability to memorize caching positions that makes it possible for them to return and retrieve the food later when males are not around

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

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

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

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

Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don‘t have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities