Anders Brodin

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.

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.

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.

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.

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.

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.

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.

Mechanisms of cache retrieval in long-term hoarding birds

Food hoarding and memory have primarily been studied in two bird families, the Corvidae (crows, jays, nutcrackers, etc.) and the Paridae (tits, titmice and chickadees). In both families there are species that hoard large quantities of seeds and nuts in the autumn and depend on these stores during the winter. Caches are concealed or highly inconspicuous and the most efficient way to retrieve them is to remember the exact locations. However, a long-term memory for a large number of caches may be physiologically expensive, and especially after long retention intervals, an alternative strategy could be to retrieve caches by cheaper but less efficient methods. Very few studies have been designed to investigate the decay of the memory in birds, but both field observations and experiments point in the same direction: although long-term hoarding corvids seem to possess an accurate long-term memory, long-term hoarding parids do not appear to. I discuss possible reasons for this and suggest that differences between the families in their degree of dependence on stored food or/and size-related limitations of brain capacity may be important.

The Effect of Dominance on Food Hoarding: A Game Theoretical Model

Many food hoarding animals live in small groups structured by rank. The presence of conspecifics in the hoarding area increases the risk of losing stored supplies. The possibility of stealing from others depends on a forager’s rank in the group. Highly ranked individuals can steal from subordinates and also protect their own caches. Since storing incurs both costs and benefits, the optimal hoarding investment will differ between individuals of different rank. In a game theoretical model, we investigate how dominant and subordinate individuals should optimize their hoarding effort. Our model imagines animals that are large‐scale hoarders in autumn and dependent on stored supplies for winter survival. Many examples can be found in the bird families Paridae and Corvidae, but the model can be used for any hoarding species that forage in groups. Predictions from the model are as follows: First, subordinates should store more than dominants, but in a predictable environment, this difference will decrease as the environment gets harsher. Under harsh conditions, dominants should store almost as much as subordinates and, later, spend almost as much time retrieving their own caches as subordinates. Second, if on the other hand, bad winter conditions were not expected when storing, dominants should spend more time pilfering caches from subordinates. Third, in populations that are highly dependent on stored supplies, dominants should store relatively more than in populations that are less dependent on stored supplies. Fourth, harsher environments will favor hoarding. And finally, if dominant individuals store, it implies that hoarders have a selfish recovery advantage over conspecific pilferers.

Changes in King Penguin breeding cycle in response to food availability

From 1991 to 1996 we investigated how the breeding cycle of King Penguins Aptenodytes patagonicus, in a small colony at South Georgia, was affected by variation in food availability between years. During the first (1992) and third (1996) of the three successful cycles studied, food was plentiful, whereas food availability was lower during the second cycle (1994). We found (1) the duration of breeding was longer (455 days) in 1994 compared to 1992 (437 days) and 1996 (438 days), (2) fewer birds made late breeding attempts in 1994 (38%) than in 1992 (88%) and 1996 (70%), and (3) those birds that made late attempts laid their egg later in 1994 (mean 16 March) compared to 1992 (19 February) and 1996 (21 February). We conclude that the breeding timetable changed in response both to the reduced availability of food in 1994 and to the subsequent improved conditions in 1996. This suggests that annual versus biennial breeding in King Penguins is dependent on the availability of food and the condition of the birds.