Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird

Knowledge of the relative importance of genetics and behavioural copying is crucial to appraise the evolvability of behavioural consistencies. Yet, genetic and non-genetic factors are often deeply intertwined, and experiments are required to address this issue. We investigated the sources of variation of adult antipredator behaviour in the Alpine swift (Apus melba) by making use of long-term behavioural observations on parents and cross-fostered offspring. By applying an 'animal model' approach to observational data, we show that antipredator behaviour of adult Alpine swifts was significantly repeatable over lifetime (r = 0.273) and heritable (h(2) = 0.146). Regression models also show that antipredator behaviours differed between colonies and sexes (females were more tame), and varied with the hour and year of capture. By applying a parent-offspring regression approach to 59 offspring that were exchanged as eggs or hatchlings between pairs of nests, we demonstrate that offspring behaved like their biological parents rather than like their foster parents when they were adults themselves. Those findings provide strong evidence that antipredator behaviour of adult Alpine swifts is shaped by genetics and/or pre-hatching maternal effects taking place at conception but not by behavioural copying.     

Foraging behaviour of the root vole Microtus oeconomus in fragmented habitats

The effect of habitat fragmentation on spatial foraging behaviour in the root vole Microtus oeconomus was investigated in seven experimental populations. Four of the populations were established in large, continuous blocks (30 × 95 m) of meadow habitat (treatment plots), whereas the three remaining populations had six small rectangular habitat fragments (30 × 7.5 m) with variable inter-fragment distances (control plots). Both the small habitat fragments and the large continuous habitat were embedded in a non-habitat matrix area which was regularly mowed. Half-way through the study period, the continuous habitat in treatment plots was destroyed by mowing to give a configuration identical to the control plots. Dyed bait placed at the edges and in the interior of habitat fragments as well as in the matrix area was used to reveal differential use of these areas for foraging. Animals in the small-fragment plots fed more than expected along the edges, while edges were used according to availability in the large blocks of continuous habitat. In the fragmented plots, the frequency of foraging in the matrix decreased with increasing distance to the fragment border and with increasing inter-fragment distances. Furthermore, the frequency of use of more than one habitat fragment in individual foraging ranges decreased with increasing inter-fragment distances. Reproductively inactive animals of both sexes fed more often along habitat edges than reproductively active animals. Reproductively active females fed exclusively in one habitat fragment, whereas inactive animals and especially reproductively active males frequently included more than one fragment in their foraging ranges. The only effect of habitat destruction was less foraging in the matrix habitat in the post-destruction treatment plots compared to the permanently fragmented control plots. This was probably an effect of different matrix quality. Root voles in these experimental populations forage in edge and matrix habitat with great risk of becoming victims to predation, and the results are interpreted in this context. Received: 19 August 1998 / Accepted: 30 June 1999     

Flight behaviour of the bird cherry aphid, Rhopalosiphum padi

Abstract Seasonal winged forms of the bird cherry aphid, Rhopalosiphum padi L., were flown in an automated flight chamber. During their maiden flights, autumn migrants (gynoparae) had a greater initial rate of climb than summer (exules) and spring migrants (emigrants). Autumn migrants, presented with a laterally-positioned green-illuminated target for 2.5 s during each minute of flight, flew for a longer period before responding to the target (110 min) than summer migrants (36 min), while spring migrants responded after an intermediate time (72 min). This period is equivalent to the migratory phase of flight. The summer migrants were maximally responsive to targets illuminated by green monochromatic light (X, 555 nm). Targets illuminated with ultraviolet (γλ 360 nm) were attractive during the migratory and green-responsive phases of flight, but infrared (γλ700 nm) wavelengths were not attractive. The results are discussed with respect to aphid behaviour in the field.     

Effects of the rearing environment on average behaviour and behavioural variation in steelhead

In the context of conservation hatcheries that seek to bolster wild populations by releasing captively-reared fishes into the wild, steelhead Oncorhynchus mykiss were used to test the hypothesis that naturalistic rearing environments promote adaptive behaviour that might otherwise not develop in typical hatchery environments. When comparisons were made among fish reared in barren, structured or structurally variable environments ( i.e. the location of the structure was repositioned every 2–3 days), structure in the rearing environment increased future exploratory behaviour, but only if the structure was stable. Under conditions of high perceived predation risk, the fish no longer exhibited increased exploratory behaviour, suggesting that it is expressed in an adaptive, context-dependant manner. Another concern with hatcheries is that relaxed selection over multiple generations in captivity can increase maladaptive behavioural variation. Compared to rearing in hatchery-typical barren environments, rearing in structured-stable environments decreased behavioural variation. This effect, which occurred during development and did not involve selection, demonstrates a different mechanism for change in behavioural variation in captivity. These experiments show that effects of structure and structural stability occur at the level of both average behaviour and behavioural variation, and suggest that these effects should be considered when fishes are reared in hatcheries for later release into the wild.     

Adaptive walks on behavioural landscapes and the evolution of optimal behaviour by natural selection

Summary One of the main challenges to the adaptationist programme in general and to the use of optimality models in behavioural and evolutionary ecology in particular is that natural selection need not optimise fitness. This challenge is addressed by considering the evolution of optimal patch choice by natural selection. The behavioural model is based on a state variable approach in which a strategy consists of a sequence denoting the patch to be visited as a function of the organism's state and time. The optimal strategy maximises expected terminal reproduction. The fitnesses of alternative strategies are computed by iteration of the associated equations for fitness; this characterises the adaptive behavioural landscape. There may be enormous numbers of strategies that have near optimal fitnesses. A population model is used to connect frequencies of behavioural types from one generation to the next. Theories on adaptive walks on fitness landscapes are considered in the context of behaviour. The main result is that within the context of optimality arguments at selective equilibrium, sub-optimal behaviours can persist. General implications for research in behavioural ecology, including tests of behavioural theories, are discussed.     

A note on the effects of co-mingling piglet litters on pre-weaning growth, injuries and responses to behavioural tests

The purpose of this study was to determine how co-mingling litters affected piglets’ pre-weaning growth, ear injuries, suckling behaviour and responses to behavioural tests used to measure coping abilities. Thirty sows and their respective litters were housed in standard farrowing crates until day 13 after birth. On day13, the partition between two neighbouring pens was removed for 20 litters allowing piglets to interact (forming 10 co-mingled litters). The remaining 10 control litters were kept in standard farrowing crates throughout the experiment. Three focal piglets from each litter were used for data collection. Focal piglets were weighed and ear injuries recorded on days 2, 4, 9, 12, 15 and 18 after birth. There were no differences in piglets’ weight gain before or after co-mingling. Ear injuries were more abundant in co-mingled litters on day 15 (P < 0.05) but these differences disappeared by day 18. Suckling behaviour was recorded on days 5, 8, 10, 14, 16 and 18 after birth. There were no differences in teat fidelity, suckling frequency and mother fidelity between treatments. Three behavioural tests, social challenge, isolation, and backtest, were performed before and after co-mingling. There were no treatment effects on piglets’ response to the isolation test and backtest. Co-mingled piglets showed longer latency for the first aggressive interaction (P < 0.05), spent more time in proximity to one another (P < 0.05) and performed less single bites (P < 0.05) than control piglets during the social challenge. In addition, the duration and frequency of aggressive interactions (P < 0.05) were lower in co-mingled piglets than control piglets. Co-mingling did not affect the frequency of single head thrusts or oral–nasal contact, but did tend to increase the frequency of escape attempts (P < 0.10). Our results suggest that co-mingling litters during lactation affects piglets’ social behaviour, by primarily decreasing aggressive interactions during social challenges.     

A note on the time budget and social behaviour of densely housed horses: A case study in Arab breeding mares

We observed a high-density herd (200 mares/ha) of 44 Arab breeding mares, while in a bare paddock in Tunisia. Twenty-minute animal focal samples and scan sampling were used to determine the time budget of the mares during the period from 9 a.m. to 3 p.m. and study their social behaviour. The data obtained reveal restricted behavioural repertoires with missing behaviour like rolling, allogrooming and lying down; unusual time budgets with a high frequency of locomotion that constitutes the most frequent activity (27.9 ± 19.47%) of the mares. Social interactions were restricted to agonistic interactions but despite the high stocking density, aggressions were not that frequent among mares.     

Ability of the desert locust (Schistocerca gregaria) to compensate for visual deprivation during the final pre‐adult and adult stages

In the desert locust (Schistocerca gregaria Forsskål), vision is a seemingly indispensable prerequisite for many behaviour patterns. The question arises as to whether and to what extent other senses can compensate for the loss of vision, and whether this can take place in the adult stage. To answer this question, both of the compound eyes of nymphs in the final pre‐adult stage are blinded (but not the ocelli), resulting in permanent visual deprivation during adult life. The results are somewhat unexpected: under laboratory conditions, in comparison with sighted controls, the blinded locusts do not exhibit any noticeable change in overall agility relative to daily activity, nor any detriment in terms of the final moult, reproductive rate or longevity. In their search for a specific food source in an experimental arena with a narrow passage between the compartment where the animals are released and the compartment containing food, in the first trial, visually deprived females need significantly more time than the sighted controls. However with an increasing number of trials, each performed after 1 day of food deprivation, the food finding latency of blinded locusts (S. gregaria) approaches or even surpasses that of normally sighted locusts. The blinded locusts use their antennae, mouthparts and tarsi more extensively, suggesting a more frequent use of tactile and chemical cues, which they gradually learn to use more efficiently. The results indicate that pre‐adult and adult S. gregaria can respond to abrupt, permanent changes in their sensory inputs, and have a significant capacity for adaptation.     

Influence of black spot disease on shoaling behaviour in female western mosquitofish, <Emphasis Type="Italic">Gambusia affinis</Emphasis> (Poeciliidae,Teleostei)

Parasites can fundamentally alter the cost–benefit ratio of living in a group, e.g. if infected individuals increase the predation risk of shoal mates. Here, the effect of an infection with a trematode, Uvulifer sp. (Diplostomatidae) on the shoaling behaviour of female western mosquitofish, Gambusia affinis, was investigated. The parasite examined causes a direct phenotypical change of the host by forming black spots on its body surface. When given a choice between a stimulus shoal and no shoal, we found shoaling tendencies to be significantly reduced in infected focal fish. In another experiment, we tested for association preferences relative to the infection status of the stimulus fish. Given the choice between an infected and a healthy stimulus fish, both infected and healthy focal fish preferred to associate with non-infected stimulus fish. Our results suggest that (1) the cost–benefit ratio of shoaling might be different for infected and non-infected individuals. Infected fish may be more affected by competition for food within a shoal. (2) Associating with infected conspecifics appears to be costly for female mosquitofish, maybe due to increased predation risk.     

Fence effects on the behavioural responses of South American fur seals to tourist approaches

Animals that breed in coastal colonies, such as pinnipeds, usually attract tourism, which can negatively affect their resting and breeding behaviour if not managed properly. One strategy to reduce human disturbance is to set up fences, but little is known about their local effectiveness. Our purpose was to assess the behavioural responses of South American fur seals (Arctocephaalus australis) towards tourist approaches before and after the implementation of fences in Cabo Polonio colony (Uruguay). We found that human disturbance levels were similar between years and that the presence of a fence reduced (1) overall fur seal responses to tourists by 60%, (2) the most intense behavioural responses (threat, attack, leaving the colony) by more than half, (3) the responses to large tourist groups (>2 people), which were the most disturbing, (4) the responses to closer (<10 m) tourist approaches, and (5) the responses involving more intrusive tourist behaviours (running, shouting, hand waving). Overall, we showed that after the erection of the fence not only human–wildlife interactions were reduced but also the most stressful fur seal behavioural responses. Although further studies are necessary, our results suggest that the implementation of fences can be a simple and affordable means of minimising human disturbance effects on pinnipeds at local levels (e.g., within colonies), particularly if combined with other strategies (e.g., changes in tourist attitudes).     

Fuelling rates of garganey ( Anas querquedula) staging in the Camargue, southern France, during spring migration

Most species of long-distance migratory birds put on energy stores to fuel their travels. However, recent studies have highlighted the potential costs associated with carrying too much fuel, either through increased predation risk or decreased flight efficiency. Consequently, it is now widely accepted that migratory birds should carry optimal rather than maximum fuel loads. Information from 372 garganey (Anas querquedula) ringed and recaptured at least once during the same spring in the Camargue, southern France, was used to document fuelling rates of individual ducks in relation to environmental variation and individual variation in condition. On average, garganey added very little fuel stores in the Camargue (mean gain per day=0.33 g, less than 0.5% of mean body-mass in total over an average stay of 5 days). Fuelling rates were negatively correlated with body mass at capture, but it cannot be excluded that this pattern was a statistical artefact. Given their body-mass at ringing, garganey could potentially still fly long distances when they stop in the Camargue. It is therefore likely that the aim of their stay in southern France is more for resting than refuelling, a finding that may have implications for the proper management of stop-over sites.Communicated by F. Bairlein     

Return migration of Atlantic Salmon in the River Tana: Phases of migratory behaviour

From a total of 174 multi-sea-winter Atlantic salmon radio tagged in the Tanafjord (northern Norway, 70°N) during 1992 and 1993, 48 Atlantic salmon were followed from entering the River Tana until spawning. Three phases were identified: (1) migratory, direct or stepwise migration to, or close to the position held at spawning; (2) search, movements both up and down river at or close to the position held at spawning; (3) holding, a period without movements prior to spawning. During the migratory phase, Atlantic salmon migrated directly to near the spawning area, or stopped between one and nine shorter periods during the upstream migration. Number of stops increased with increasing migratory distance in 1993, but no such correlation was found in 1992. The highest migratory speeds were recorded in the lower parts of the river. A distinct change in migratory pattern was found in 67% of the Atlantic salmon near or at the area held at spawning. Most common was a search phase of erratic movements with more than one down river movement. After the movement terminated, 96% of the Atlantic salmon had a period when no or little movement was recorded until spawning (on average 55 days in 1992 and 51 days in 1993). There was no preference for staying at, up or down river from the spawning area during this holding period. Early ascending Atlantic salmon migrated to spawning areas further from the mouth than the later arriving Atlantic salmon in 1993, but not in 1992. The proportion of time spent on the migratory phase increased, while the proportion of time spent on the holding phase decreased with increasing distance to the spawning area.     

Predatory behaviour of common kestrels (Falco tinnunculus) in the wild

The predatory behaviour of eight wild adult common kestrels (Falco tinnunculus) was recorded during predatory tests carried out in the wild under controlled conditions. Those birds were offered one laboratory mouse each, which was restrained on a base, thereby simulating natural predation. The predatory sequence was recorded directly, but also video-taped. The sequence was rather homogeneous among the kestrels, with most kestrels starting the attack glide from a perch, then capturing the prey at high speed. The mouse was grabbed directly, upon landing; in one instance, however, it disentangled from the bird’s foot and was captured after a few seconds. The target was usually grabbed at the shoulders or neck, or at the trunk. Soon after capture the kestrel flew to a distant perch, where it usually stroked the prey with one single peck, before starting ingestion, which began about 1 min time after prey grasping. Our results are the first to show the possibility of maintaining standardized conditions to study the predatory behaviour of birds of prey. As they are very similar to those obtained in previous tests carried out in captivity using rehabilitated kestrels, our results also confirm earlier ones showing that the kestrel’s predatory behaviour is rather stereotyped—i.e. performed with limited variation—and that it can be studied reliably even in captivity.     

Carrying food items to cover for consumption: the behavior of ten bird species feeding under the risk of predation

Summary In earlier work (Lima et al. 1985; Lima 1985), we found that gray squirrels (Sciurus carolinensis) and black-capped chickadees (Parus atricapillus) when exploiting a patch of food in the open often carried individual food items to protective cover for consumption. Their tendency to carry (i) decreased as distance of the patch from cover increased, and (ii) increased as size of the available food items increased. A simple model indicated that this behavior was consistent with a trade-off between efficient foraging and predation risk. Maximal feeding efficiency was achieved by always eating at the patch, whereas minimal time exposure to predators was achieved by carrying all items to cover for consumption. Because predation-riskrelated trade-offs are likely to be of importance in the determination of feeding behavior, we surveyed the behavior of 10 bird species feeding under similar conditions to assess both the generality of the above results and the adequacy of some simple assumptions concerning the assessment and perception of predation risk.We observed considerable interspecific variability in behavior. Of the 10 species studied, 4 behaved in a manner similar to the squirrels and chickadees. Five other species showed an increased tendency to carry with larger items but no clear tendency to decrease carrying from longer distances. The one remaining species exhibited neither behavioral trend.The model that predicted squirrel and chickadee behavior failed to account for all observed behavior. The behavior of all species, however, was influenced by predation risk, and the discrepancy between theory and observation most likely reflects shortcomings of the model. These discrepancies indicate that other factors, in addition to exposure time, may be of significance in the perception of predation risk by several (or all) of the species studied. Of particular importance may be a distance-dependent probability of escaping attack. Other results indicate that predation risk may influence handling times via aspects of the digestive process.     

A high‐density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour

High‐density SNP microarrays (“SNP chips”) are a rapid, accurate and efficient method for genotyping several hundred thousand polymorphisms in large numbers of individuals. While SNP chips are routinely used in human genetics and in animal and plant breeding, they are less widely used in evolutionary and ecological research. In this article, we describe the development and application of a high‐density Affymetrix Axiom chip with around 500,000 SNPs, designed to perform genomics studies of great tit (Parus major) populations. We demonstrate that the per‐SNP genotype error rate is well below 1% and that the chip can also be used to identify structural or copy number variation. The chip is used to explore the genetic architecture of exploration behaviour (EB), a personality trait that has been widely studied in great tits and other species. No SNPs reached genomewide significance, including at DRD4, a candidate gene. However, EB is heritable and appears to have a polygenic architecture. Researchers developing similar SNP chips may note: (i) SNPs previously typed on alternative platforms are more likely to be converted to working assays; (ii) detecting SNPs by more than one pipeline, and in independent data sets, ensures a high proportion of working assays; (iii) allele frequency ascertainment bias is minimized by performing SNP discovery in individuals from multiple populations; and (iv) samples with the lowest call rates tend to also have the greatest genotyping error rates.     

The congener; A neglected area in the study of behaviour

This paper seeks a deeper understanding of the congener as a factor in animal and human behaviour. It does so, not by concentrating on analyses of stimulus exchanges - largely specific to the species - by which a congener is recognized, but on the more general questions of why a notion of congener exists at all and why it plays such an extraordinary important role in animal and human behaviour.Three separate approaches, by way of anthropomorphic psychology, a paraphysical energy model and the physical theory of the implicate order, lead to the recognition of a certain inseparability of self and congener; and to an interpretation of the content of the notion of congener and of the behaviour in relation to it, in terms of the fundamental concept of energy and the even more fundamental one of order.Dedicated to Professor Gerard P. Baerends, one of my valued guides in ethology.     

Modelling changes in migration pattern of herring: collective behaviour and numerical domination

According to the adopted-migrant hypothesis, first time spawning herring Clupea harengus learn their migration pattern from schooling with older individuals. Changes in migration pattern of Norwegian spring-spawning herring co-occur with the recruitment of abundant year classes to the spawning stock. It is argued that this is due to the abundant year classes being unable to learn from the older ones since most of the recruiting year class only experience their own naïve class-mates. An individual-based school simulation study is presented to explore the hypothesis. Behaviour is simulated using individual rules that take into account the movements of nearby individuals. After establishing a schooling pattern, a small proportion of the individuals is directed to move towards a given position while the remaining individuals keep using their behaviour rules. When <4% of the individuals are so directed there is no response seen in the remaining school. But when ≥7% of the total school is directed to a specific location, the remaining individuals always respond and follow the directed individuals. The simulations thus show that determined individuals can have a substantial influence on the collective behaviour of schools. Furthermore, the knife-edge response in school behaviour suggests that the relative abundance of determined individuals in a school plays an important part in the collective behaviour. This mechanism can explain the observed changes in migration pattern of Norwegian spring-spawning herring associated with the recruitment of abundant year classes to the adult Stock.     

Developmental trends in mother-infant interactions in Java macaques (Macaca fascicularis) during the first ten days of life

In this study on Java macaques themain characteristics of the mother-infant relationship during infants' first 10 days have been elaborated. Early mother and infant behaviour is described and early interactions between mothers and their young have been analyzed. Observations and trend analyses of early behaviours like ventro-ventral contact behaviour, being on nipple, and explorative behaviour, make it clear that Java macaque infants play an important role in the early development of mother-infant interactions. In contrast to the rhesus and the stumptailed infant, the young Java macaque appears to develop a great variety of behaviours in its first 10 days. Whereas the infant's behaviour gains in complexity and social initiative, the mother becomes increasingly more passive and self-oriented. Early mother-infant interaction can be characterized by mutual adjustment.     

Testing multiple hypotheses for the maintenance of male homosexual copulatory behaviour in flour beetles

Diverse animal groups exhibit homosexual interactions, yet the evolutionary maintenance of such behaviours remains enigmatic as they do not directly increase reproductive success by generating progeny. Here, we use Tribolium castaneum flour beetles, which exhibit frequent male homosexual copulations, to empirically test several hypotheses for the maintenance of such behaviours: (1) establishing social dominance; (2) practice for future heterosexual encounters; and (3) indirect sperm translocation. We found no evidence that Tribolium males use homosexual copulations either to establish dominance or to practice behaviours that increase their subsequent heterosexual reproductive performance. Our results provide limited support for the hypothesis of indirect sperm translocation: when males from two genetic strains mated with females immediately following a homosexual copulation, females produced progeny sired not only by the directly mating male, but also by that male’s homosexual partner. However, this phenomenon was detected in only 7% of homosexual pairs, and in each case such indirectly sired progeny accounted for < 0.5% of females’ total progeny. Direct observations indicated that mounting males often released spermatophores during homosexual copulations. These observations suggest that homosexual copulations may be a behavioural mechanism that allows males to expel older, potentially low‐quality sperm. Additional work is needed to test this new hypothesis, and to determine whether sperm release during homosexual copulations occurs in other groups.