Microsatellite variation in the yellowhammer Emberiza citrinella: population structure of a declining farmland bird.

In recent years, there has been much concern in the UK about population declines of widespread species in agricultural habitats. Conservation-orientated research on declining birds has focused on vital rates of survival and productivity. However, the environmental factors which may influence movements between populations of widespread species is poorly understood. Population genetic structure is an indirect description of dispersal between groups of individuals. To attempt to develop an understanding of genetic structuring in a widespread, but declining, farmland bird, we therefore investigated the yellowhammer, Emberiza citrinella, population in England and Wales using microsatellite data. Our first aim was to investigate whether there was genetic substructuring in the population. A second aim was to investigate if there was a relationship between genetic distances and various environmental variables. Finally, we analysed the microsatellite data for evidence of loss of genetic variation due to population decline. Our data showed a slight but significant structure within the yellowhammer population. This therefore cannot be considered a panmictic population. Our example from South Cumbria implies that high-altitude barriers may have a slight influence on population structure. However, on the whole, genetic distances between sample sites were not significantly correlated with geographical distances, degrees of population connectivity, high altitudes, or differences in precipitation between sites. Finally, we detected departures from mutation-drift equilibrium (excess heterozygosity), which is indicative of a loss of genetic variation through recent decline.

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.

Science, uncertainty and policy: food for thought.

The organisation and work of the Food Standards Agency are described. The Agency is a new non-Ministerial Government department with responsibility for protecting the health of the public and other interests of consumers in relation to food. Its roles encompass assessment of risk (through scientific expert committees) as well as risk communication and management. Among the many changes that the Agency has brought about is a new commitment to openness. All policy discussions and decisions take place in public. Diet and bovine spongiform encephalopathy are used as examples to illustrate the Agency's approaches to dealing with risk and uncertainty.

Neurochemical evidence for at least two regional subdivisions within the homing pigeon (Columba livia) caudolateral neostriatum.

The distributions of one neurotransmitter, two neurotransmitter-related substances, and five neuropeptides were examined within the homing pigeon caudolateral neostriatum (NCL). All eight neuroactive substances were found within a tyrosine hydroxylase (TH)-dense region that defines the NCL. Overall regional variation in the relative density of these substances suggested at least two neurochemically distinct portions of NCL. Dorsal NCL contained relatively dense staining for TH, choline acetyltransferase, and substance P, whereas vasoactive intestinal polypeptide was more abundant in ventral portions of NCL. Serotonin and cholecystokinin were found to be densest in intermediate portions of NCL. Somatostatin and leucine-enkephalin were homogeneously distributed throughout NCL. The results suggest that NCL may consist of multiple subdivisions. Investigations into the behavioral importance of these regions are necessary to clarify the role of this brain region in avian behavior.

Hippocampal tissue transplants reverse lesion-induced spatial memory deficits in zebra finches (Taeniopygia guttata).

The avian hippocampal formation (Hf) plays an important role in spatial memory for food storing. Here we examined the effects of excitotoxic lesions of the Hf and subsequent neural transplantation on a one-trial associative memory task in zebra finches. The results showed (1) that small ibotenic acid lesions of the dorsal Hf of zebra finches produced significant spatial memory impairments compared with controls, sham-lesioned birds, and prelesion performance; and (2) that Hf-lesioned birds given transplants of embryonic hippocampal (H) tissue, but not those given transplants of embryonic anterior telencephalon (AT) tissue, showed a significant reversal of the performance deficits on the spatial memory task. Lesioned-only birds and lesioned birds given H or AT transplants that did not survive did not show behavioral improvement. Sham-lesioned and untreated control birds maintained good performance throughout the experiment. The H and AT transplants were found to be growing partially within the Hf and partially within the underlying ventricle. The transplants appeared healthy and contained neurons with beaded and unbeaded fibers (shown by immunohistochemistry with antibodies to parvalbumin, substance P, and a 200 kDa neurofilament protein). Blood vessels and erythrocytes were also present within the transplants. The results show that neural transplants can survive within the bird brain and that small lesions of the Hf produce significant spatial memory deficits that can only be reversed by surviving homologous H transplants, and not by heterologous telencephalon transplants.

Spatial learning induces neurogenesis in the avian brain.

It is known from previous work that neurones are born continuously in the ventricular zone of the bird brain. In this study, we show that the amount of cell proliferation in the ventricular zone of the hippocampus (HP) and the hyperstriatum ventrale (HV) is influenced by behavioural experience. Two groups of birds (marsh tits) were compared: those allowed to store and retrieve food once every 3 days between days 35 and 56, and age-matched controls treated in an identical way, except that they were not allowed to store and retrieve food. After three trials of storing and retrieval, between days 35 and 41 posthatch, experienced birds showed a significantly higher rate of cell proliferation than did controls. The experienced birds also showed a significant increase in total cell and neuronal number by day 56 posthatch, after eight trials of storing and retrieval. There were no significant differences in the amount of programmed cell death in the hippocampus in this study. In a novel analysis of the data we demonstrate that the effect of experience between days 35 and 41 was to increase the daily rate of neurogenesis in the ventricular zone from 3.9 to 10%, and that this change could account for the increase in total hippocampal neuronal number by day 56 in the experienced birds. Thus, the observed increase in hippocampal volume and neuronal number as a result of food storing and retrieval, may be caused by an increase in neurogenesis in the first few trials of food storing experience.

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.

Efferent connectivity of the hippocampal formation of the zebra finch (Taenopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin.

The avian hippocampal formation (HP) is considered to be homologous to the mammalian hippocampus, being involved in memory formation and spatial memory in particular. The subdivisions and boundaries of the pigeon hippocampus have been defined previously by various morphological methods to detect further similarities with the mammalian homologue. We studied the efferent projections of the zebra finch hippocampus by applying Phaseolus vulgaris leucoagglutinin, and three main subdivisions were distinguished on the basis of the connectivity patterns. Dorsolateral injections gave rise to projections innervating the rostralmost extension of the HP, a laminar complex including the dorsal and ventral hyperstriata and the lamina frontalis superior, the rostral lobus parolfactorius, the medial and ventral paleostriatal regions, the lateral septal nucleus, the nucleus of the diagonal band, the dorsolateral corticoid area, the archistriatum posterius, and the nucleus taeniae in the telencephalon. In the diencephalon, labelled axons were seen in the periventricular and lateral hypothalamus, including the lateral mammillary nuclei, and in the dorsolateral and the dorsomedial posterior thalamic nuclei, whereas, in the midbrain, only the area ventralis of Tsai contained hippocampal fibres. With the exception of the bilateral archistriatal efferents, all projections were ipsilateral. Dorsomedial injections gave rise to a local fibre system that was almost completely restricted to the ipsilateral hippocampal formation. In addition, lectin-containing fibres continued in the dorsal septal region and a thin band in the hyperstriatum accessorium, adjacent to the lateral ventricle. Ventral injections gave rise to axons innervating ipsilaterally the dorsolateral subdivision, and bilaterally the medial septal nuclei and the contralateral ventral hippocampus.

The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study.

Neurones in the zebra finch dorsal forebrain (hippocampal and lateral corticoid complexes) were described and located using Golgi methods. We distinguish two main classes of neurones, spinous with distant projecting axons, and aspinous with local axons. Spinous neurones are subclassified into bitufted pyramids, localised in the medial hippocampus, modified bitufted pyramids in the intermediate corticoid area, multipolar neurones in the parahippocampal area, lateral hippocampus and corticoid complex, and stellate neurones in the corticoid complex. Among the aspinous neurones, we distinguish neurones with basket axons, dense pericellular axons, radial axons, and net-like axons, and horizontal cells seen in the dorsolateral corticoid area. This group includes sparsely spinous neurones found in the intermediate corticoid area. On the basis of the neuronal characteristics, we divide the hippocampal complex into 5 fields: medial and lateral hippocampus, parahippocampal area, central field of the parahippocampal area, and crescent field. The lateral corticoid complex is subdivided into an intermediate corticoid area and a dorsolateral corticoid area. We conclude that the avian dorsal forebrain is an assembly of fields interconnected by axonal collaterals. The medial hippocampus and possibly the intermediate corticoid area display a primitive cortex-like organisation, whereas the other fields lack any sign of cortical structure.

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.

Discrimination and recognition of photographs of places by homing pigeons.

Operant studies on pigeons using slide-projected images suggest that photographs of geographical locations might be used as a research tool to study the importance of visual landmarks in homing. Before using this method, however, it is necessary to show that pigeons do see photographic slides as representing real world locations. After reviewing the evidence for picture-to-object correspondence for geographical locations in pigeons, we report the results of an experiment designed to test whether outdoor experience at a location affected homing pigeons' ability to categorise slides of that versus another location displayed in an operant set-up. Four birds visited one location immediately before each experimental session; four birds visited an irrelevant location. No effect of outdoor experience was found on acquisition, or transfer to novel stimuli. The possible reasons for limitations on picture-to-object correspondence are discussed.

Effects of photoperiod on food-storing and the hippocampus in birds.

Birds that store food have a relatively large hippocampus compared to non-storing species. The hippocampus shows seasonal differences in neurogenesis and volume in black-capped chikadees (Parus atricapillus) taken from the wild at different times of year. We compared hippocampal volumes in black-capped chickadees captured at the same time but differing in food-storing behaviour because of manipulations of photoperiod in the laboratory. Differences in food-storing behaviour were not accompanied by differences in the volume of the hippocampus. Hippocampal volumes also did not differ between two groups of a non-food-storing control species, house sparrows (Passer domesticus), exposed to the same conditions as the chickadees.

Memory in food-storing birds: from behaviour to brain.

As a result of natural history studies, it has been hypothesized that food-storing birds may develop a special kind of memory to cope with the demand imposed by their food-storing behaviour (i.e. the ability to retrieve food from a wide variety of stores over varying amounts of time after storage). Recent studies on food-storing birds suggest that, at a relatively late stage in their development, the specific memories associated with food-storing behaviour can stimulate growth of the hippocampus, an area of the brain concerned with memory processing.

Hippocampal growth and attrition in birds affected by experience.

Hand-raised marsh tits (Parus palustris) were exposed to experience of storing and retrieving food at three different ages (35-59, 60-83, 115-138 days posthatch). At equivalent ages, control birds were given identical experience except for storing and retrieving food. Volumetric analysis was carried out to measure the hippocampal region, ectostriatum, and telencephalon of experienced and control birds. Individuals with experience of storing and retrieving food had a larger hippocampal region relative to the rest of the telencephalon than did controls, independent of age. The hippocampal region of experienced birds also contained more neurons and fewer apoptotic cells than that of controls. No volumetric differences were observed in ectostriatum, which served as a control brain region. The results suggest that some aspect of food-storing and retrieval directly influences growth and attrition of the hippocampal region in food-storing birds.

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.

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.

Histochemical distribution of zinc in the brain of the zebra finch (Taenopygia guttata).

The distribution of zinc was studied in the brain of the zebra finch (Taenopygia guttata) by means of the selenium histochemical method. A specific pattern was seen, which usually correlated with the main known architectonic subdivisions. In addition, a few as yet unidentified structures were observed. In the telencephalon, the pallial components were stained with moderate to strong intensity. The only exceptions were the hyperstriatum intercalatus superior, a small medial area in the hyperstriatum accessorium and in the dorsolateral cortex, and the dorsomedial part of the hippocampal complex, which were virtually devoid of staining. Staining of the dorsal ventricular ridge components varied considerably. The archistriatum, the nucleus accumbens, the nucleus of the stria terminalis, the hyperstriatum ventrale and the lateral septum showed moderate to strong staining. The medial septum was weakly stained. The neostriatum showed a rather complex pattern of staining with unstained areas, such as the magnocellular nucleus of the anterior neostriatum, and other parts intensely stained, especially in its caudal region. Both paleostriatii primitivum and augmentatum showed a rostro-caudal gradient that was increasingly stained. We also observed an intensely stained area ventral to the fasciculus prosencephali lateralis and lateral to the tractus septomesencephalicus, a weakly to moderately stained band ventral to the lobus parolfactorius, an intensely stained zone along the lateral ventricle in the hyperstriatum ventrale, and an unstained almond-shaped nucleus in the lateral hyperstriatum ventrale. In the diencephalon, the hypothalamus showed a moderate to strong, rather uniform staining, whereas the thalamus was usually weakly to moderately stained, with the exception of a few unstained nuclei. Only the lateral nucleus of the habenula was stained, and with strong intensity. Most of the mesencephalon stained rather uniformly with a moderate to strong intensity. The most intense staining was seen in the substantia grisea centralis, the substantia grisea et fibrosa periventricularis, the torus semicircularis and the nucleus intercollicularis. The tectum opticum was virtually devoid of stain except for two light bands in the stratum griseum et fibrosum superficiale. The formatio reticularis was moderately stained. All the other structures were either weakly stained or unstained. Some staining was seen in the Purkinje and the granular layers of the cerebellum, as well as around its internal nuclei. The pons and the medulla oblongata showed an overall moderate to intense staining, with the exception of a few unstained nuclei. When compared in three bird species belonging to different genera, zinc distribution shows remarkable similarities, despite species, age and methodological differences.(ABSTRACT TRUNCATED AT 400 WORDS)

A subpopulation of large calbindin-like immunopositive neurones is present in the hippocampal formation in food-storing but not in non-storing species of bird.

The avian hippocampal formation (HP) is thought to play a role in the processing of spatial memory related to food-storing behaviour. The HP of two food-storing species (marsh tit (Parus palustris) and magpie (Pica pica)) and two non-storing species (great tit (Parus major) and jackdaw (Corvus monedula)) were compared following calbindin-like immunostaining. In the dorsal hippocampal region, both species of food-storing birds had larger calbindin-immunoreactive cells than did the two non-storing species. The fact that this association between storing behaviour and cell morphology is seen in two unrelated families of birds, the Paridae (marsh tit versus great tit) and Corvidae (magpie versus jackdaw) suggests that there may be a direct link between food-storing behaviour and the dorsal hippocampal calbindin-immunoreactive cell population.