Dietrich von Holst

The concept of stress and its relevance for animal behavior

Publisher Summary This chapter discusses the significance of the stress concept in gaining a better understanding of social mechanisms in nonhuman mammals. The development of this concept during the past years and the resulting present understanding of different stress reactions are described in the chapter. The triggers of stress reactions are mainly psychical processes resulting from the assessment of a situation by an individual. Dependent on the coping behavior of the individual, these processes lead to different physiological response patterns, which can result in a number of pathophysiological effects. The chapter introduces the most important currently applied methods in assessing stress levels in animals. Particular attention is paid to methodological problems, as well as to the limits of interpretation. The focal points of the chapter are the sympathetico–adrenomedullary and pituitary–adrenocortical systems, the pituitary–gonadal axis, and the immune system. An overview of the relationships between social situations and stress responses is provided, in which the research focuses on the monogamous and territorial tree shrews and the polygamous and territorial European wild rabbits. In these cases, the social rank of an individual, its sociopositive interactions with conspecifics, and the stability of the social system are determinants in the effects of a social situation on the individuals vitality and fertility.

Behavioural and physiological responses of naïve European rabbits to predator odour

Animals show a variety of antipredator strategies in response to the presence of chemical cues from mammalian predators. Nevertheless, there is no general agreement as to whether recognition of predator odours is dependent upon experience. We conducted an experiment on European rabbits Oryctolagus cuniculus naive to any contact with predators and we investigated (1) whether they possessed a mechanism for the recognition of the odour of a predator, and (2) how they responded behaviourally and physiologically to that odour. We used fox Vulpes vulpes faeces as the source of the predator odour and sheep Ovis aries faeces as a nonpredator control odour. The experiments were conducted in small outdoor enclosures where the animals were kept singly. We recorded patterns of vigilance, activity and feeding, and changes in glucocorticoids and body mass. The rabbits showed a clear antipredator response to the presence of fox faeces, whereas they behaved neutrally in response to sheep odour. The response consisted of increased avoidance and vigilance while feeding and more investigation before feeding. Furthermore, the rabbits showed a physiological alarm response, that is, an increased responsiveness of their adrenocortical system and weight loss. However, the total activity budget, measured as time spent outside the burrow, the time spent feeding, and the amount of food ingested remained largely stable during the experiment. We conclude that rabbits recognised predator odours and that this recognition was independent of experience.

Social Rank, Stress, Fitness, and Life Expectancy in Wild Rabbits

Abstract Wild rabbits of the two sexes have separate linear rank orders, which are established and maintained by intensive fights. The social rank of individuals strongly influence their fitness: males and females that gain a high social rank, at least at the outset of their second breeding season, have a much higher lifetime fitness than subordinate individuals. This is because of two separate factors: a much higher fecundity and annual reproductive success and a 50% longer reproductive life span. These results are in contrast to the view in evolutionary biology that current reproduction can be increased only at the expense of future survival and/or fecundity. These concepts entail higher physiological costs in high-ranking mammals, which is not supported by our data: In wild rabbits the physiological costs of social positions are caused predominantly by differential psychosocial stress responses that are much lower in high-ranking than in low-ranking individuals.

Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator

Summary.Stress has been widely studied in different mammals, but the physiological stress reaction that the odour of a predator could induce in preys has not received much attention. Besides, not all the animals would respond to the same extent to a known stressor.We developed an experimental procedure with eleven naïve European rabbits (Oryctolagus cuniculus) in order to determine the individual physiological response to the olfactory detection of a potential predator. The rabbits were housed singly in small enclosures with a concrete burrow system and food and water were available ad libitum. The animals followed a control trial, without odour, and an experimental trial where we confronted the rabbits with fox (Vulpes vulpes) odour. Furthermore, another sample of eleven rabbits followed a control procedure subjected to the same housing and handling procedures but without facing the predator odour. In order to assess the physiological response we analysed the concentration of glucocorticoid metabolites in the faeces of the rabbits. Therefore, everyday faecal samples were collected and analysed with an enzyme immunoassay in order to measure the corticosterone metabolites (CM), particularly, those metabolites with a 5α-3β, 11β-diol structure.After validating the assay for wild rabbits, we found that the simulated presence of a predator (fox odour) in the enclosure resulted in an increase in faecal CM concentrations. However, the stressor did not affect all the animals in the same way. We found a general increase in the individual differences. In particular, males experienced a higher increase than females, though the overall response was similar for both sexes.To our knowledge this is one of the first attempts to analyse the assessment of the risk of predation by means of non-invasive methods.

Organization of Territorial Marking Behavior by Testosterone During Puberty in Male Tree Shrews

According to current hypotheses, in mammals male-specific behavior is organized perinatally, and activated in adulthood by male gonadal hormones. However, this strict differentiation between early organizational and late activational hormone effects has been criticized recently. Around puberty the testosterone levels of male mammals rise far above adult levels. In this study we examined the relevance of this pubertal testosterone peak on marking behavior of adult tree shrews (Tupaia belangeri). Male tree shrews were castrated before puberty and treated with testosterone either around puberty or in adulthood. Several months later, the marking behavior of the castrated adult animals was examined in standard tests in different scent conditions before and after a second testosterone treatment. Males castrated as adults as well as fertile females were used as controls. The testosterone peak during puberty did not influence male marking behavior in the absence of scent from conspecifics (familiarization marking) or in the presence of female scent (sexual marking). However, testosterone during puberty determined both the male-specific reaction patterns to male scent (territorial marking) and the male-specific regulation of this behavior by testosterone. These results indicate that testosterone during puberty specifically organizes male territorial-marking behavior. To our knowledge, these are the first results demonstrating organizational effects of testosterone during puberty on male behavior.

Major histocompatibility complex variation and age‐specific endoparasite load in subadult European rabbits

Genes of the major histocompatibility complex (MHC) play a fundamental role in the vertebrate immune response and are amongst the most polymorphic genes in vertebrate genomes. It is generally agreed that the highly polymorphic nature of the MHC is maintained through host–parasite co‐evolution. Two nonexclusive mechanisms of selection are supposed to act on MHC genes: superiority of MHC heterozygous individuals (overdominance) and an advantage for rare MHC alleles. However, the precise mechanisms and their relative importance are still unknown. Here, we examined MHC dependent parasite load in European rabbits (Oryctolagus cuniculus) from a distinct population with low MHC diversity (three alleles, six genotypes). Using a multivariate approach, we tested for associations of individual MHC class II DRB constitution and the rabbits’ intestinal burden with nematodes and coccidia. Rabbits having a particular allele showed lower infestations with hepatic coccidia (E. stiedai). However, a comparison of all six genotypes in the population revealed that carriers of this allele only benefit when they are heterozygous, and furthermore, MHC heterozygosity in general did not affect individual parasite load. In conclusion, this study suggests an immunogenetic basis of European rabbit resistance to hepatic coccidiosis, which can strongly limit survival to maturity in this species. Our study gives a complex picture of MHC–parasite correlations, unveiling the limits of the classical hypotheses of how MHC polymorphism is maintained in natural systems.

Characterisation of MHC class II DRB genes in the northern tree shrew ( Tupaia belangeri )

Genes of the major histocompatibility complex (MHC) mainly code for proteins of the immune system of jawed vertebrates. In particular, MHC class I and II cell surface proteins are crucial for the self/non-self discrimination of the adaptive immune system and are the most polymorphic genes in vertebrates. Positive selection, gene duplications and pseudogenes shape the face of the MHC and reflect a highly dynamic evolution. Here, we present for the first time data of the highly polymorphic MHC class II DRB exon 2 of a representative of the mammalian order scandentia, the northern tree shrew Tupaia belangeri. We found up to eight different alleles per individual and determined haplotype constitution by intensively studying their inheritance. The alleles were assigned to four putative loci, all of which were polymorphic. Only the most polymorphic locus was subject to positive selection within the antigen binding sites and only alleles of this locus were transcribed.

Long-term effects of litter sex ratio on female reproduction in two iteroparous mammals

Summary 1. Female mammals that develop in male-biased litters show signs of masculinization because they are exposed to the testosterone produced by their male siblings in utero. The early exposure to testosterone can affect female morphology, physiology, behaviour and life-history traits. 2. Masculinization is commonly seen as the collateral effect of developing in a male-biased litter. However, when resources are limiting, masculinization might be adaptive because androgenized females could monopolize resources. 3. We investigated whether females from male-biased litters, and therefore likely to be masculinized, showed adaptive advantages under different competing scenarios. For that, we used data from two long-term field projects studying yellow-bellied marmots (Marmota flaviventris Audubon and Bachman, 1841) and European rabbits (Oryctolagus cuniculus Linnaeus, 1758). We explored whether litter sex composition affected fitness-related reproductive traits: the onset of breeding, offspring production and the probability of reproduction in a given year. 4. Our study shows long-term consequences of litter sex composition on reproduction in European rabbits and yellow-bellied marmots. Females from male-biased litters from both species delayed the onset of breeding, suggesting the maladaptive nature of masculinization. However, in European rabbits, this effect was density-dependent. Under higher-density conditions, female rabbits from male-biased litters brought forward the onset of breeding, which might increase the probability of offspring overwinter survival and therefore their fitness. These females under limiting conditions might have a higher resource holding potential. 5. We conclude that prenatal maternal effects in natural populations should be taken into account when studying life-history variation. Moreover, it is notable that small variations in naturally occurring prenatal exposure to androgens have profound impacts on individuals, social groups and the population structure.

Weather Effects on Reproduction, Survival, and Body Mass of European Rabbits in a Temperate Zone Habitat

Understanding the effects of environmental factors on the dynamics of animal populations is one of the major challenges for population biologists. In particular, the impact of climate and weather has been the focus of many studies during the last years (e.g., Lima and Jaksic 1998; Milner et al. 1999; Stenseth 1999; Yoccoz and Stenseth 2000; Aars and Ims 2002; Lande et al. 2003). However, data on specific effects of the weather on different vital rates are rare, because, in small mammals in particular, individually based studies are difficult to conduct, and long-term datasets are needed for obtaining reliable results. The European rabbit Oryctolagus cuniculus is an interesting and very suitable model organism for such a study. Formerly restricted to a relict distribution on the Iberian Peninsula about 3,000 years ago, this species has been spread by man over nearly all continents and to different climatic zones (Flux 1994). This species is characterized by a high reproductive capacity (e.g., Myers and Poole 1962; Goncalves et al. 2002; von Holst et al. 2002) but also by high mortality rates, in particular in juveniles (e.g., Richardson and Wood 1982). This can result in strong short-term fluctuations in population numbers (e.g., Erlinge et al. 1984; Myers and Poole 1963). Furthermore, several studies on European rabbit populations point out, that climatic and weather conditions have a strong impact on the abundance and on population densities of this small mammal (e.g., Erlinge et al. 1984; Trout et al. 2000; Schropfer et al. 2000; Calvete et al. 2004). Since 1988 we have kept and studied a population of European rabbits in a field enclosure of 2 ha in Upper Franconia, Germany. In this chapter, we review our findings about the effects of weather on different reproductive components, on the body mass of juveniles at the end of the vegetation period, and the over-winter survival of adults and first-year individuals’ reproduction, survival, and body mass. Many aspects presented here have been described in our previous papers, however not all results have been published.

Auswirkungen sozialer Kontakte bei Säugetieren

Säugetiere leben in Sozialverbänden, die sich zwar von Tierart zu Tierart beträchtlich unterscheiden, für die einzelne Art jedoch außerordentlich konstant sind ‐ von Formen, bei denen die Individuen einzeln oder paarweise in begrenzten Revieren leben, bis hin zu Formen, die in streng hierarchisch gegliederten Gruppen in weiten Gebieten umherziehen. Aufrechterhalten werden diese Sozial‐systeme durch den ständigen Kontakt gesünder, der Tiere untereinander, wobei dieser nicht nur das Verhalten der Individuen, sondern auch ihre Gesundheit und Fruchtbarkeit entscheidend beeinflussen kann, wie besonders eindrucksvoll Untersuchungen australischer Beuteltiere der Gattung Antechinus zeigen. Diese in Australien weit verbreitete Tiergattung (Breitfußbeutelmäuse) ernährt sich vorwiegend von Insekten und kleineren Wirbeltieren. All bisher untersuchten Arten haben einen extrem synchronisierten Lebenszyklus: Ende September – im australischen Frühling – bekommen die Weibchen Junge, die bis zum Januar entwöhnt werden, doch noch einige Monate friedlich mit ihren Müttern zusammenleben. Ende Mai verlassen die Jungen ihren Geburtsort und verteilen sich in ihrem Lebensraum. Im August – dem australischen Winter – setzt dann die kurze Fortpflanzungsperiode ein: Auf der Suche nach Weibchen durchstreifen die Männchen ihr Gebiet und werden hierbei ständig in heftige Kämpfe mit anderen Männchen verwickelt. Nach zwei bis drei Wochen – und damit stets vor Erreichen ihres ersten Lebensjahres – sterben dann alle Männchen. Die Weibchen überleben und bringen nach einer Tragzeit von etwa einem Monat ihre Jungen zur Welt – Männchen und Weibchen: Ein neuer Zyklus beginnt [64].