Treating hummingbirds as feathered bees: a case of ethological cross-pollination.

Hummingbirds feed from hundreds of flowers every day. The properties of these flowers provide these birds with a wealth of information about colour, space and time to guide how they forage. To understand how hummingbirds might use this information, researchers have adapted established laboratory paradigms for use in the field. In recent years, however, experimental inspiration has come less from other birds, and more from looking at other nectar-feeders, particularly honeybees and bumblebees, which have been models for foraging behaviour and cognition for over a century. In a world in which the cognitive abilities of bees regularly make the news, research on the influence of ecology and sensory systems on bee behaviour is leading to novel insights in hummingbird cognition. As methods designed to study insects in the laboratory are being applied to hummingbirds in the field, converging methods can help us identify and understand convergence in cognition, behaviour and ecology.

Dairy cow feeding space requirements assessed in a Y-maze choice test.

The effect of proximity to a dominant cow on a low-ranking cow's willingness to feed was assessed using choice tests. The main aim of the experiment was to determine the feeding space allowance at which the majority of subordinate cows would choose to feed on high-palatability food (HPF) next to a dominant cow rather than feeding alone on low-palatability food (LPF). Thirty Holstein-Friesian cows were used in the study. Half of the cows were trained to make an association between a black bin and HPF and a white bin and LPF, and the other half were trained with the opposite combination. Observations of pair-wise aggressive interactions were observed during feeding to determine the relative social status of each cow. From this, dominant and subordinate cows were allocated to experimental pairs. When cows had achieved an HPF preference with an 80% success rate in training, they were presented with choices using a Y-maze test apparatus, in which cows were offered choices between feeding on HPF with a dominant cow and feeding on LPF alone. Four different space allowances were tested at the HPF feeder: 0.3, 0.45, 0.6, and 0.75 m. At the 2 smaller space allowances, cows preferred to feed alone (choices between feeding alone or not for 0.3- and 0.45-m tests were significantly different). For the 2 larger space allowances, cows had no significant preferences (number of choices for feeding alone or with a dominant). Given that low-status cows are willing to sacrifice food quality to avoid close contact with a dominant animal, we suggest that the feeding space allowance should be at least 0.6m per cow whenever possible. However, even when space allowances are large, it is clear that some subordinate cows will still prefer to avoid proximity to dominant individuals.

Restoring depleted coral-reef fish populations through recruitment enhancement: a proof of concept.

To determine whether enhancing the survival of new recruits is a sensible target for the restorative management of depleted coral-reef fish populations, settlement-stage ambon damsel fish Pomacentrus amboinensis were captured, tagged and then either released immediately onto small artificial reefs or held in aquaria for 1 week prior to release. Holding conditions were varied to determine whether they affected survival of fish: half the fish were held in bare tanks (non-enriched) and the other half in tanks containing coral and sand (enriched). Holding fish for this short period had a significantly positive effect on survivorship relative to the settlement-stage treatment group that were released immediately. The enrichment of holding conditions made no appreciable difference on the survival of fish once released onto the reef. It did, however, have a positive effect on the survival of fish while in captivity, thus supporting the case for the provision of simple environmental enrichment in fish husbandry. Collecting and holding settlement-stage fish for at least a week before release appear to increase the short-term survival of released fish; whether it is an effective method for longer-term enhancement of locally depleted coral-reef fish populations will require further study.

A role for nonapeptides and dopamine in nest-building behaviour.

During nest building in zebra finches (Taeniopygia guttata), several regions in the social behaviour network and the dopaminergic reward system, which are two neural circuits involved in social behaviour, appear to be active in male and female nest-building finches. Because the nonapeptides, mesotocin and vasotocin and the neurotransmitter, dopamine, play important roles in avian social behaviour, we tested the hypothesis that mesotocinergic-vasotocinergic and dopaminergic neuronal populations in the social behaviour network and dopaminergic reward system, respectively, are active during nest building. We combined immunohistochemistry for Fos (an indirect marker of neuronal activity) and vasotocin, mesotocin or tyrosine hydroxylase on brain tissue from nest-building and non-nest-building male and female zebra finches and compared Fos immunoreactivity in these neuronal populations with the variation in nest-building behaviour. Fos immunoreactivity in all three types of neuronal populations increased with some aspect of nest building: (i) higher immunoreactivity in a mesotocinergic neuronal population of nest-building finches compared to controls; (ii) increased immunoreactivity in the vasotocinergic neuronal populations in relation to the amount of material picked up by nest-building males and the length of time that a male spent in the nest with his mate; and (iii) increased immunoreactivity in a dopaminergic neuronal population in relation to the length of time that a male nest-building finch spent in the nest with his mate. Taken together, these findings provide evidence for a role of the mesotocinergic-vasotocinergic and dopaminergic systems in avian nest building.

Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds.

Song and brain structure are compared amongst 41 species of oscine birds by using the method of independent evolutionary contrasts. We find a significant correlation between the relative volume of the song control centre, the high vocal centre (HVC), and the number of song types typically found in the repertoire. Relative HVC volume is not correlated with the number of different syllable types per song bout. The relative volume of a second song nucleus, area X, is not significantly correlated with either measure. Relative HVC volume is uncorrelated with relative volume of the hippocampus, a brain area involved in other forms of memory. This is the first evidence for repeated independent evolution of an association between complexity of learned song and the relative volume of one of the song control nuclei though to be involved in song learning.

Spatial working memory in rats: no differences between the sexes.

In a number of mammalian species, males appear to have superior spatial abilities to females. The favoured explanations for this cognitive difference are hormonal, with higher testosterone levels in males than females leading to better spatial performance, and evolutionary, where sexual selection has favoured males with increased spatial abilities for either better navigational skills in hunting or to enable an increased territory size. However, an alternative explanation for this sex difference focuses on the role of varying levels of oestrogen in females in spatial cognition (the 'fertility and parental care' hypothesis). One possibility is that varying oestrogen levels result in variation in spatial learning and memory so that, when tested across the oestrous cycle, females perform as well as males on days of low oestrogen but more poorly on days of high oestrogen. If day in the oestrous cycle is not taken into account then, across an experiment, any sex differences found would always produce male superiority. We used a spatial working memory task in a Morris water maze to test the spatial learning and memory abilities of male and female rats. The rats were tested across a number of consecutive days during which the females went through four oestrous cycles. We found no overall sex differences in latencies to reach a submerged platform in a Morris water maze but, on the day of oestrus (low oestrogen), females took an extra swim to learn the platform's location (a 100% increase over the other days in the cycle). Female swim speed also varied across the oestrous cycle but females were no less active on the day of oestrus. These results oppose the predictions of the fertility and parental care hypothesis.

Development of hippocampal specialisation in a food-storing bird.

Previous studies demonstrated that amongst food-storing passerine birds the hippocampal region (dorso-medial cortex) is enlarged relative to the rest of the telencephalon. It has been hypothesised that this hippocampal specialisation is related to the spatial memory requirements of retrieving large numbers of stored items. Here we compare the development of the hippocampus in a food-storing and a non-storing corvid, the adults of which differ in relative hippocampal volume. The volume, cell density and number of cells in the hippocampal region of nestling (5-25 days post hatching) and adult (> 320 days old) magpies Pica pica (food-storing) and jackdaws Corvus monedula (non-storing) were measured. In both species the volume of the hippocampus increases with the volume of the rest of the telencephalon during the nestling growth phase. The relative volume of the hippocampus in 5- to 25-day-old nestlings of the two species does not differ significantly. In the food-storing magpie, the relative volume of the adult hippocampus is significantly larger than that of nestlings, whilst in the jackdaw, adults and nestlings do not differ. The density of neurons declines with increasing age and this effect is more marked in jackdaws than in magpies. Neuron number did not change significantly with age, but is significantly greater in adult magpies than in adult jackdaws. These results are discussed in relation to the possibility that changes in hippocampal volume and cell number are related to the use of spatial memory in retrieving stored food.

Hippocampal volume in migratory and non-migratory warblers: effects of age and experience.

We tested the hypothesis that experience of migration from Europe to tropical Africa by Garden Warblers is associated with changes in the relative volume of the hippocampus, a brain region thought to be involved in processing spatial information, including that used in navigation. Relative hippocampal volume was larger in birds at least one year old that had migrated to and from Africa, than in naive birds approx. 3 months old. Further comparisons between groups of differing age and experience of migration suggested that both experience and age during the first year have an effect of relative hippocampal volume. The increase in relative hippocampal volume was mainly due to a decrease in the size of the telencephalon; however, the comparison between young, naive birds and older, experienced birds also suggests a possible increase in absolute hippocampal volume. The latter is associated with an increase in number and density of neurons, whilst the former is associated with an increase in density but no change in total number of neurons. In a non-migratory close relative of the garden warbler, the Sardinian warbler, older birds had a smaller telencephalon but there was no change in hippocampal volume, which supports the view that changes in the hippocampus may be associated with migratory experience, whilst changes in the telencephalon are not.

Development of hippocampal specialisation in two species of tit (Parus spp.).

Food storing birds have been shown to have a larger hippocampus, relative to the rest of the telencephalon, than do non-storers. A previous study reported that this difference in relative hippocampal volume is not apparent in a comparison of nestling birds, but emerges after birds have fledged. This conclusion was based on a comparison of a storing and a non-storing species in the corvid family. The present study compared another storer/non-storer pair of species in order to test whether the results of the previous study can be replicated in another family of birds. The volumes of the hippocampal region and remainder of the telencephalon were measured and estimates of neuron size, density and total number in the hippocampal region were made for nestlings and adults of the food-storing marsh tit Parus palustris and non-storing blue tit Parus caeruleus. Relative hippocampal volume did not differ between nestlings of the two species, whilst the relative hippocampal volume of adult marsh tits was greater than that of blue tits. The difference between adults arose because in marsh tits but not blue tits, adults had a significantly larger relative hippocampal volume than did nestlings. Neuron density was significantly higher in both species in nestlings than in adults and adult blue tits had fewer neurons than did adult marsh tits. The results of this study are largely consistent with the earlier study comparing a storing and non-storing species of corvid, suggesting that the observed patterns may reflect a general difference between storers and non-storers in the development of the hippocampal region.

Explanations for variation in cognitive ability: Behavioural ecology meets comparative cognition.

Sara Shettleworth has played a defining role in the development of animal cognition and its integration into other parts of biology, especially behavioural ecology. Here we chart some of that progress in understanding the causes and importance of variation in cognitive ability and highlight how Tinbergen's levels of explanation provide a useful framework for this field. We also review how experimental design is crucial in investigating cognition and stress the need for naturalistic experiments and field studies. We focus particularly on the example of the relationship among food hoarding, spatial cognition and hippocampal structure, and review the conflicting evidence for sex differences in spatial cognition. We finish with speculation that a combination of Tinbergen and Shettleworth-style approaches would be the way to grapple with the as-yet unanswered questions of why birds mimic heterospecifics.

Delayed-matching-to-sample by marsh tits and great tits.

The ability of two species of tits to remember the location and/or features of an object was tested in a delayed-matching-to-sample procedure. Three values of retention interval between presentation of the sample stimulus and the choice--30 sec, 5 min, and 15 min--were used. Both species performed at above-chance level at all retention intervals, and there was no significant decline in accuracy with increasing interval. A pool of 100 stimulus objects was used, but the results of control trials indicated that the birds responded primarily to location rather than stimulus features of the object itself. Although the food-storing marsh tit tended to perform at a higher level than the non-storing great tit, the only significant difference between the species was in the first 50 trials of the first treatment, when the birds were acquiring the task. The results are discussed in relation to the hypothesized special memory capacity of food-storing birds.

Food storing and the hippocampus in Paridae.

Food storing passerines have a larger hippocampus, relative to the rest of the telencephalon and/or body mass, than do non-storing species. This study looked at the relationship between relative size of the hippocampus and degree of food storing in six species of Paridae (blue tit, Parus caeruleus, great tit, P major, marsh tit, P palustris, coal tit, P ater, black-capped chickadee, P. atricapillus, and willow tit, P montanus). The degree of storing by these species varies from little or none to thousands of food items. The period over which food is stored also varies from a few hours to several months. The results showed that hippocampal volume, relative to the rest of the telencephalon, is larger in those species that store more food, store for longer, or both. In an analysis of intraspecific variation within two of the species, the food storing marsh tit and the non-storing blue tit, there was a significant positive relationship between hippocampal volume relative to body mass, and telencephalic volume relative to body mass, in the marsh tit but no relationship between these variables in the blue tit.

A larger hippocampus is associated with longer-lasting spatial memory.

Volumetric studies in a range of animals (London taxi-drivers, polygynous male voles, nest-parasitic female cowbirds, and a number of food-storing birds) have shown that the size of the hippocampus, a brain region essential to learning and memory, is correlated with tasks involving an extra demand for spatial learning and memory. In this paper, we report the quantitative advantage that food storers gain from such an enlargement. Coal tits (Parus ater) a food-storing species, performed better than great tits (Parus major), a nonstoring species, on a task that assessed memory persistence but not on a task that assessed memory resolution or on one that tested memory capacity. These results show that the advantage to the food-storing species associated with an enlarged hippocampus is one of memory persistence.

Hippocampal specialization of food-storing birds.

In a study of 52 individuals belonging to 35 species or subspecies of passerine birds it was shown that the volume of the hippocampal complex relative to brain and body size is significantly larger in species that store food than in species that do not. Retrieval of stored food relies on an accurate and long-lasting spatial memory, and hippocampal damage disrupts memory for storage sites. The results suggest, therefore, that food-storing species of passerines have an enlarged hippocampal complex as a specialization associated with the use of a specialized memory capacity. Other life-history variables were examined and found not to be correlated with hippocampal volume.