Septum volume and food‐storing behavior are related in parids

The hippocampal formation (HF) of food‐storing birds is larger than non‐storing species, and the size of the HF in food‐storing Black‐Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non‐storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food‐storing Black‐Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non‐storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black‐Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food‐storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food‐storing birds, may be specialized for some aspects of food‐storing and spatial memory. © 2002 Wiley Periodicals, Inc. J Neurobiol 51: 215–222, 2002     

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.     

Greater hippocampal neuronal recruitment in food-storing than in non-food-storing birds

Previous research has shown heightened recruitment of new neurons to the chickadee hippocampus in the fall. The present study was conducted to determine whether heightened fall recruitment is associated with the seasonal onset of food-storing by comparing neurogenesis in chickadees and a non-food-storing species, the house sparrow. Chickadees and house sparrows were captured in the wild in fall and spring and received multiple injections of the cell birth marker bromodeoxyuridine (BrdU). Birds were held in captivity and the level of hippocampal neuron recruitment was assessed after 6 weeks. Chickadees showed significantly more hippocampal neuronal recruitment than house sparrows. We found no seasonal differences in hippocampal neuronal recruitment in either species. In chickadees and in house sparrows, one-third of new cells labeled for BrdU also expressed the mature neuronal protein, NeuN. In a region adjacent to the hippocampus, the hyperpallium apicale, we observed no significant differences in neuronal recruitment between species or between seasons. Hippocampal volume and total neuron number both were greater in spring than in fall in chickadees, but no seasonal differences were observed in house sparrows. Enhanced neuronal recruitment in the hippocampus of food-storing chickadees suggests a degree of neurogenic specialization that may be associated with the spatial memory requirements of food-storing behavior.     

The seasonal hippocampus of food-storing birds

Food storing is seasonal in birds like chickadees, nuthatches and jays, occurring at high levels in fall and winter and low levels in spring and summer. Memory for cache sites is hippocampus dependent in chickadees and both the recruitment of new neurons into the hippocampus and the total size of the hippocampus change seasonally. Unlike seasonal change in the vocal control nuclei of songbirds, however, change in the hippocampus appears not to be controlled by photoperiod. The annual timing of hippocampal neuronal recruitment and change in hippocampal size is quite variable, reaching maximum levels at different times of year in different studies. The amount of food-storing activity by chickadees is known to be influenced by flock dominance structure, energy balance, food availability, and other seasonally varying factors. The variable timing of seasonal change in the hippocampus may indicate that the hippocampus of food-storing birds changes annually in response to change in the intensity of food storing behaviour itself.     

Food resource matching by foraging tits Parus spp. during spring-summer in a Mediterranean mixed forest; evidence for an ideal free distribution

We analysed whether patterns of microhabitat use by Blue Tits Parus caeruleus , Great Tits Parus major and Crested Tits Parus cristatus inhabiting a mixed forest consistently matched the patterns of food availability experienced by foraging birds during spring-summer. The use of five microhabitats by each bird species (the foliage of three tree species, shrubs and ground) and the availability of food in trees during the prebreeding, breeding and post-breeding periods of the birds' annual cycle were measured. All three tit species foraged mainly in the outer part of tree canopies (small branches and leaves or needles). Tit distributions between tree species matched food resource distributions irrespective of overall food resource levels, which varied four-fold between the study periods, and tit species. Tits also exploited secondary microhabitats (shrubs and ground) in periods of low food availability; Blue Tits tended to use shrubs, whereas Great and Crested Tits foraged on the ground. Between-trees distributions fitted that expected from an ideal free distribution, suggesting that food availability and intraspecific exploitative competition were the main factors governing tree use by tits. In contrast, patterns of use of secondary microhabitats (shrubs and ground) seemed to indicate a role for the species-specific morphological configurations of each tit species since Blue Tits are better adapted to hang and tended to forage in shubs, whereas Great and Crested Tits are better adapted to feed on horizontal surfaces and tended to forage on the ground. No evidence of interspecific interactions was observed. Overall, the results pointed to an independent exploitation of Mediterranean mixed forest by each bird species, food availability and food accessibility being the main factors affecting microhabitat use by foraging tits.     

Food-storing birds: adaptive specialization in brain and behaviour?

Among the passerine birds, species that store food have an enlarged hippocampal region (dorso-medial cortex), relative to brain and body size, when compared with the non-storers. The volume of one of the major afferent-efferent pathways (the septo-hippocampal pathway) is also greater in food storing species. This specialization of brain structure is discussed in relation to behavioural studies in which the spatial memory of storing and non-storing species has been compared.     

Memory for spatial and object-specific cues in food-storing and non-storing birds

Two storer/non-storer pairs of species, marsh tit (Parus palustris)/blue tit (P. caeruleus) and jay (Garrulus glandarius)/jackdaw (Corvus monedula) were compared on a one-trial associative memory task. In phase I of a trial birds searched for a reward in one of four feeders which differed in their trial-unique spatial location and object-specific cues. Following a retention interval, the birds had to return to the same feeder to obtain a further reward. In control trials the array of feeders was unaltered, whilst in dissociation tests it was transformed to separate spatial location and object-specific cues.In control trials there was no difference in performance between species. In dissociation tests, the two storing species went first to the correct spatial location and second to the correct object-specific cues, whereas the two non-storing species went first with equal probability to the correct spatial and local object cues.Monocular occlusion was used to investigate differences between the two eye-systems. In control trials there was no effect of occlusion. In dissociation trials, all 4 species preferentially returned to the feeder with the correct object-specific cue when the left eye had been covered in phase I and to the feeder in the correct spatial position when the right eye had been covered in phase I.These results suggest that (a) food-storing birds differ from non-storers in responding preferentially to spatial information and (b) in storers and non-storers the right eye system shows a preference for object-specific cues and the left eye system for spatial cues.     

Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: the black-capped chickadee

The volume of the hippocampal formation (HF) in black-capped chickadees (Poecile atricapillus) varies across the seasons, in parallel with the seasonal cycle in food hoarding. In this study, we estimate cell density and total cell number in the HF across seasons in both juveniles and adults. We find that the seasonal variation in volume is due to an increase in the number of small and large cells (principally neurons) in the fall. Adults also have lower neuron densities than juveniles. Both juveniles and adults show an increase in cell density in the rostral part of the HF in August and a subsequent decrease toward October. This suggests that the net cell addition to the HF may already start in August. We discuss the implications of this early start with respect to the possibility that the seasonal change in HF volume is driven by the experience of food hoarding. We also speculate on the functional significance of the addition of neurons to the HF in the fall.     

Memory and Brain in Food‐Storing Birds: Space Oddities or Adaptive Specializations?

Scatterhoarding birds that cache food items have become an important model system for the study of spatial memory and its correlates in the brain. In particular, it has been suggested that through adaptive specialization, species that cache food have better spatial memory and a relatively larger hippocampus than their non-caching relatives. Critics of this approach, dubbed neuroecology, maintain that neither of these hypotheses has been confirmed. Here, we review the evidence pertaining to a correlation between food-storing capability and the relative volume of the hippocampus. Hippocampal volume has been related to food-storing behaviour in comparisons between species, within species, or within individuals, but the evidence is not consistent. There are several possible reasons for this inconsistency, including: (1) food-hoarding birds may not always use memory for retrieval, (2) there may be systematic differences between data from North American and Eurasian species that affect the analysis, and (3) sample sizes have in many cases been too small. In addition, both the independent variable (degree of food-hoarding specialization) and the dependent variable (relative volume of the hippocampus) are not clearly and consistently defined. Alternatively, it is possible that the neuroecological hypothesis is false. Systematic empirical research is necessary to determine whether or not food-storing birds have evolved adaptive specializations in brain and cognition.     

Advantages of social foraging of Willow Tits Parus montanus

The mean number of Willow Tits Parus montanus in single-species flocks was significantly larger than in mixed-species flocks of Willow and Coal Tits P. ater. Both flock size and the tendency of Willow Tits to join mixed-species flocks were negatively correlated with ambient temperature, probably because each bird, when the metabolic rate of the birds increased, could allocate more time to foraging due to improved predator detection by many eyes. The vigilance time of Willow Tits decreased with flock size and was determined by the total number of individuals in a flock rather than by the number of Willow Tits in mixed-species flocks of Willow and Coal Tits.     

Seasonal changes in hippocampus size and spatial behaviour in mammals and birds

Hippocampus is involved in processing of environmental spatial information, and its size is known to correlate positively with spatial abilities in mammals and birds. Comparisons between species suggest that amount of spatial information processed (the mean area of home range in particular) is related with hippocampus size. Do seasonal and age changes in hippocampus size correlate with seasonal dynamics of spatial behaviour during ontogenesis? The data obtained through observational and experimental studies confirm the possibility that hippocampus size may be subjected to adaptive modifications along with cyclic changes in spatial behavior. In course of seasonal dynamics, strong positive correlation was found between hippocampus mass, home range size, and mobility of small mammals. Recently, first facts demonstrating seasonal changes of hippocampus and spatial behaviour (in connection with food-storing and brood parasitism) were found in birds. A lot of facts obtained for different taxonomical groups shows parallel seasonal changes in spatial behaviour and morphology of brain region functionally related to such behaviour. Thus, in adult birds and mammals, not only behaviour but also brain structure is phenotypically flexible in response to seasonally changing environment. Morphophysiological mechanisms of hippocampus seasonal changes are also discussed.     

不同纬度洞巢鸟类对人工巢箱的利用及差异

迄今对洞巢鸟类生活史特征的纬度变异（特别是热带洞巢鸟类的繁殖）了解还十分有限。我们于2018年3至8月,分别在海南吊罗山（热带）、河南董寨（亚热带）和河北塞罕坝（温带）的林缘地带,悬挂相同规格的人工巢箱招引洞巢鸟类繁殖,用以比较不同地理区域的洞巢鸟类对人工巢箱的利用情况及其孵化成效和繁殖成功率。野外共悬挂577个木制巢箱,3个研究地的利用率在海南吊罗山为最低（32.6%）,河南董寨最高（92.0%）。3个地点均有大山雀（Parus cinereus）入住（占总巢数的84.3%）,其孵化成效和繁殖成功率在3个地点不存在显著差异（P > 0.05）。但在河北塞罕坝,大山雀的孵化成效（75.7%）和繁殖成功率（65.7%）显著低于同域繁殖的褐头山雀（Poecile montanus）（97.7% 和97.7%）和煤山雀（Periparus ater）（93.5%和90.3%）（P < 0.05）。研究表明,3个地理区域利用巢箱繁殖的洞巢鸟的种类、数量以及对巢箱的利用率均存在差异,但对于广布种大山雀来说,地理位置的差异并不影响其孵化成效和繁殖成功率。     

Photoperiodic regulation of food storing and hippocampus volume in black-capped chickadees, Poecile atricapillus

In seasonal environments animals organize their behaviour around annual cycles of resource availability. Wild black-capped chickadees are most likely to hoard food in autumn. At this time of year chickadees are also reported to have a larger hippocampus, a brain area important for spatial memory. This study examined how photoperiodic condition affects these seasonal changes. Captive chickadees were exposed to one of three treatments. Photorefractory birds were held on long days (19:5 h light:dark) and had small gonads. Photosensitive birds were held on short days (LD 9:15 h) and also had small gonads. Photostimulated birds were switched from short to long days and quickly entered breeding condition with large gonads. Photosensitive birds (on short days) stored more seeds than photorefractory birds (on long days). Photostimulated birds stored seeds at a high rate when on short days, but reduced storing when transferred to long days. These results indicate that long days inhibit storing regardless of gonadal condition. There were no differences between groups in hippocampal volume, indicating that photoperiod can produce changes in food-storing behaviour without affecting hippocampal size. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Seasonal changes in neuron numbers in the hippocampal formation of a food‐hoarding bird: The black‐capped chickadee

The volume of the hippocampal formation (HF) in black‐capped chickadees (Poecile atricapillus) varies across the seasons, in parallel with the seasonal cycle in food hoarding. In this study, we estimate cell density and total cell number in the HF across seasons in both juveniles and adults. We find that the seasonal variation in volume is due to an increase in the number of small and large cells (principally neurons) in the fall. Adults also have lower neuron densities than juveniles. Both juveniles and adults show an increase in cell density in the rostral part of the HF in August and a subsequent decrease toward October. This suggests that the net cell addition to the HF may already start in August. We discuss the implications of this early start with respect to the possibility that the seasonal change in HF volume is driven by the experience of food hoarding. We also speculate on the functional significance of the addition of neurons to the HF in the fall. © 2000 John Wiley & Sons, Inc. J Neurobiol 44: 414–422, 2000     

Carotenoid plumage hue and chroma signal different aspects of individual and habitat quality in tits

We hypothesized that Blue Tits Cyanistes caeruleus and Great Tits Parus major from low quality habitat (small woods) would have less yellow ventral plumage than those from high quality habitat (large woods) because they moult faster and/or their diet contains fewer carotenoids. They moult faster because they moult later in the season and are subject to more rapidly shortening daylengths. We tested this using a database of the plumage coloration (chroma, hue and lightness) of birds breeding in woods of different sizes, by manipulating the speed of moult in captive Blue Tits, and by counting the abundance and size of caterpillars (the major source of dietary carotenoids) in the diet of nestlings. In accordance with our hypothesis, juveniles of both species (which moult about three weeks later than adults) were about 8% less saturated in colour (lower chroma) than adults, but there was no significant difference in chroma between habitats. However, both species did differ significantly in hue between large and small woods. Blue Tits forced to moult faster in captivity, at a rate similar to that caused by a month's delay in the start of moult, had yellow flank feathers that were 32% less saturated in colour than those allowed to moult more slowly. Blue Tit nestlings in large woods consumed 47% more caterpillar flesh (per gram of faecal material voided) than those in small woods, and Great Tit pulli 81% more. When habitat effects were controlled for in ANOVAs, Blue Tits mated assortatively on the basis of flank hue and Great Tits on the basis of flank lightness. Flank colour therefore has the capacity to provide information about the potential quality of both habitats, and individual birds, to potential colonists and sexual partners.     

Seeing without being seen: a removal experiment with mixed flocks of Willow and Crested Tits Parus montanus and cristatus

This paper tests the hypothesis that foraging site selection reflects a trade-off between the various needs for concealment from predators, to find food, and for the individual to maintain some view of its surroundings. After removal of Crested Tits Parus cristatus (the dominant species in mixed flocks), Willow Tits P. montanus did not decrease their foraging heights as expected but remained in the most exposed parts of young pines. In contrast, after removal of Willow Tits, Crested Tits increased their foraging height from the sheltered lower canopy to sites previously occupied by Willow Tits. When flock size was reduced, the birds maintained the same high levels of vigilance without concealing themselves in dense vegetation. I suggest that flock members may benefit from foraging in sites that afford good anti-predator vigilance.     

Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis)

This study investigates the effects of captivity and testosterone treatment on the volumes of brain regions involved in processing visual and spatial information in adult dark-eyed juncos (Junco hyemalis). We treated captive and free-living male juncos with either testosterone-filled or empty implants. Captive juncos had a smaller hippocampal formation (HF) (both in absolute volume and relative to telencephalon) than free-living birds, regardless of hormone treatment. Testosterone-treated males (both captive and free-living) had a smaller telencephalon and nucleus rotundus, but not a smaller HF or ectostriatum, than controls. We found that free-living testosterone-treated males had larger home ranges than free-living controls in agreement with earlier experiments, but we found no corresponding difference in HF volume. We discuss the implications of the effect of captivity on HF volume for past and future laboratory experiments.     

The effect of habitat quality on foraging patterns, provisioning rate and nestling growth in Corsican Blue Tits Parus caeruleus

Many bird species face seasonal and spatial variation in the availability of the specific food required to rear chicks. Caterpillar availability is often identified as the most important factor determining chick quality and breeding success in forest birds, such as tits Parus spp. It is assumed that parents play an important role in mediating the effect of environment on chick development. A reduction in prey availability should therefore result in increased foraging effort to maintain the amount of food required for optimal chick development. To investigate the capacity of adults to compensate for a reduction in food supply, we compared the foraging behaviour of Blue Tits Parus caeruleus breeding in rich and poor habitats in Corsica. We monitored the foraging effort of adults using radiotelemetry. We also identified and quantified prey items provided to nestlings by using a video camera mounted on the nest. We found that the mean travelling distance of adults was twice as great in the poor habitat as it was in the rich. Despite the marked difference in foraging distance, the proportion of optimal prey (caterpillars) in the diet of the chicks and the total biomass per hour per chick did not differ between the two habitats. We argue that relationships between habitat richness, offspring quality and breeding success cannot be understood adequately without quantifying parental effort.     

Observations on the breeding behaviour of the Stripe‐breasted tit (Parus fasciiventer) in Bwindi Impenetrable National Park,Uganda

The motivation of this study was to investigate some hitherto unknown information on the breeding ecology of the Stripe‐breasted Tit (Parus fasciiventer) in Bwindi Impenetrable National Park, south‐western Uganda. Parus fasciiventer is one of the least studied and endemic bird species restricted to the montane forests of the Albertine Rift. Regionally, it is classified as near‐threatened. The study was carried out around the Institute of Tropical Forest Conservation Ruhija camp and the period of study was from January to June 2003. Data were generated through direct observation at the nest box sites of three active nests. Each of the nest boxes was monitored from the time of nest building to the time the chicks fledged. Results and comparative assessments from this study demonstrate that P. fasciiventer, compared with its temperate congeners like Great Tits (Parus major), Marsh Tits (Parus palustris), Crested Tits (Parus cristatus), Coal Tits (Parus ater) and Blue Tits (Parus caeruleus), raised small broods and had longer nestling period. The findings further revealed that the species is capable of raising more than one brood in a single breeding season and provide further evidence that it is a cooperative breeder. Parents participated equally in raising the young, an indication of pure parenting in the species.     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.