Opening the Black Box of Developmental Experiments: Behavioural Mechanisms Underlying Long‐Term Effects of Early Social Experience

Typically, animals spend a considerable portion of their time with social interactions involving mates, offspring, competitors and group members. The social performance during these interactions can strongly depend on the social environment individuals have experienced early in life. Despite a considerable number of experiments investigating long‐term effects of the early social environment, our understanding of the behavioural mechanisms mediating these effects is still limited, mainly for two reasons. (1) Only in few experimental studies have researchers actually observed and quantified the behaviour of their study animals during the social treatment. (2) Even if differences in social interactions between social rearing treatments are reported, these differences might not be causally linked to any observed long‐term effects later in life. The aim of this review was to investigate whether behavioural records of animals during the experimental manipulation of their social environment can help (1) identifying behavioural mechanisms involved in a long‐term effect and (2) obtaining a better understanding of the long‐term consequences of early manipulations. First, I review studies that manipulated the social environment at an early stage of the ontogeny, observed the social interactions and behaviour during the social experience phase and subsequently tested the performance in social and non‐social behavioural tasks at a later life stage. In all reviewed studies, treatment differences were reported both in social interactions during the social experience phase and in social and/or non‐social behaviours later in life. Second, I discuss four classes of behavioural mechanisms that can cause the reported long‐term effects of social experience, namely learning by experience, social learning, sensory stimulation and social cueing. I conclude that social interactions during the social experience phase should always be recorded for at least two reasons. Knowledge about how the social interactions differ between rearing treatments (1) permits researchers to formulate hypotheses about candidate mechanisms causing long‐term effects on behaviour and (2) can help to interpret unexpected outcomes of developmental experiments. Finally, I propose that as a crucial ultimate step towards understanding effects of the early social environment, we should develop targeted experiments testing for the causality of identified candidate mechanism.     

Behaviour and welfare of veal calves fed different amounts of solid feed supplemented to a milk replacer ration adjusted for similar growth

Veal calves in Europe are typically fed large quantities of milk replacer and small amounts of solid feed, a diet known to lead to the development of abnormal oral behaviours in these animals. These abnormal oral behaviours are thought to be an indication of frustration, chronic stress, and hence poor welfare. The present study investigated how different feeding strategies, differing in solid feed and milk replacer provision, affected the behaviour and welfare of veal calves across time. Four treatment groups (A–D) comprising of 12 Holstein–Friesian bull calves each (7.6 ± 0.1 weeks old and 54.7 ± 0.3 kg at arrival), penned in groups of three, were fed one of four amounts of a solid feed mixture, i.e. 50% concentrates, 25% fresh maize silage, and 25% wheat straw (on dry matter [DM] basis): A = 0, B = 9, C = 18, and D = 27 g DM/kg^0.75/d. Provision of milk replacer was adjusted to achieve similar average daily gain across treatments. Behaviour was recorded around feeding (10 min continuous focal observations of individual calves) and throughout the day (7 sessions of 30 min scan sampling at 5 min interval every 2 h from 06:30 h) every week for four months. In an attempt to find an easy practical method to measure behavioural response to feeding strategy, two 3-min behavioural tests were carried out: (1) in months 1 and 3, calves were presented with a ball and latency to make oral contact with it was recorded; and (2) in month 1, calves were presented with an overall and time spent orally manipulating (i.e. chewing or licking) it was recorded using scan sampling every 10 s. Calves in treatment D displayed less abnormal oral behaviours around feeding, less tongue playing throughout the day, and more chewing in the first two months, compared to treatment A. Treatment B only led to lower tongue playing levels compared to A and treatment C had no benefit in terms of reducing abnormal oral behaviours. Although a solid feed dose–response was expected on the display of abnormal behaviours in veal calves, treatment C did not fit within this expectation. These findings point to a more complex relationship between solid feed and abnormal oral behaviour frequency in veal calves. The two behavioural tests distinguished the different treatments as expected, and thus showed a solid feed dose–response. Because of an increase in chewing and ruminating efficiency over time, amounts of solid feed should be increased with age to maintain high levels of chewing and ruminating. Moreover, high levels of chewing and ruminating may have to be maintained long enough at the beginning of the fattening period to lead to a reduction in abnormal oral behaviours.     

Fractal Long‐Range Correlations in Behavioural Sequences of Wild Chimpanzees: a Non‐Invasive Analytical Tool for the Evaluation of Health

Quantitative evaluation of health impairments in wild chimpanzees was explored using fractal long‐range correlations of behavioural sequences. The health status of 13 chimpanzees in the Mahale Mountains National Park, Tanzania was evaluated non‐invasively using standard behavioural observation and parasitological analysis of stool samples. Based on these data, individuals were classified as being either healthy or sick. Behavioural sequences were analysed and shown to exhibit long‐range power law correlations. The behavioural sequences of individuals in healthy and sick states were quantitatively evaluated using detrended fluctuation analysis of social and non‐social behaviours within behavioural sequences. These values were compared and significant differences in long‐range correlations were found between health states. Sex differences were also noted, with female social behaviour displaying a larger fractal dimension than male social behaviour. The fractal dimension of females declined significantly in sick individuals. This analysis of behaviour provides a new and effective non‐invasive method to record and evaluate the general state of health and related stress of animals in the wild. Possible applications of this method in captive situations include the monitoring and evaluating of stress levels over time.     

Behavioural and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates

This study investigates the behavioural and neural mechanisms involved in the oviposition behaviour of the turnip root fly,Delia floralis (Fallen). Behavioural studies showed that glucosinolates modulated the oviposition behaviour of the flies on artificial leaves as well as the number of eggs laid in the soil at the base of these leaves. Electrophysiological responses to glucosinolates were obtained from type A and type D sensilla on the prothoracic and mesothoracic tarsi, as well as from the long contact sensilla on the labellum. The neural responses from these sensilla were positively correlated with the oviposition behaviour of the flies and with the number of eggs laid. Of the eleven glucosinolates tested in the behavioural and electrophysiological tests, the flies were most responsive to glucobrassicanapin, gluconapin and glucobrassicin. The type D tarsal sensilla were more responsive to the glucosinolates than either the type A tarsal sensilla or the labellar sensilla. The structure-activity investigations showed that slight modifications to the chemical composition of the glucosinolates resulted in changes in neural activity.     

Risk, resources and state-dependent adaptive behavioural syndromes

Many animals exhibit behavioural syndromes-consistent individual differences in behaviour across two or more contexts or situations. Here, we present adaptive, state-dependent mathematical models for analysing issues about behavioural syndromes. We find that asset protection (where individuals with more 'assets' tend be more cautious) and starvation avoidance, two state-dependent mechanisms, can explain short-term behavioural consistency, but not long-term stable behavioural types (BTs). These negative-feedback mechanisms tend to produce convergence in state and behaviour over time. In contrast, a positive-feedback mechanism, state-dependent safety (where individuals with higher energy reserves, size, condition or vigour are better at coping with predators), can explain stable differences in personality over the long term. The relative importance of negative- and positive-feedback mechanisms in governing behavioural consistency depends on environmental conditions (predation risk and resource availability). Behavioural syndromes emerge more readily in conditions of intermediate ecological favourability (e.g. medium risk and medium resources, or high risk and resources, or low risk and resources). Under these conditions, individuals with higher initial state maintain a tendency to be bolder than individuals that start with low initial state; i.e. later BT is determined by state during an early 'developmental window'. In contrast, when conditions are highly favourable (low risk, high resources) or highly unfavourable (high risk, low resources), individuals converge to be all relatively bold or all relatively cautious, respectively. In those circumstances, initial differences in BT are not maintained over the long term, and there is no early developmental window where initial state governs later BT. The exact range of ecological conditions favouring behavioural syndromes depends also on the strength of state-dependent safety.     

Assessing Short‐ and Long‐Term Repeatability and Stability of Personality in Captive Zebra Finches Using Longitudinal Data

Assessing behavioural consistency is crucial to understand the evolution of personality traits. In the present study, we examined the short‐ and long‐term repeatability and stability of two unrelated personality traits – exploratory tendencies and struggling rate – using captive female zebra finches ( Taeniopygia guttata). We performed two experimental sessions of behavioural tests with a 7‐mo interval, which represents up to one quarter of a zebra finch's life expectancy. We showed that, overall, exploratory tendencies and struggling rate were significantly repeatable in the short term. However, only exploratory tendencies were repeatable in the long term. We found interindividual differences in short‐term stability of exploratory tendencies, but not struggling rate, providing evidence for differences in intraindividual variability. In the long term, struggling rate significantly decreased between the two experimental sessions, whereas exploratory tendencies remained stable. Finally, the amount of interindividual variation measured at both sessions did not differ. Our results suggest that short‐ and long‐term repeatability and stability of personality may vary between individuals, depending on the behavioural trait under scrutiny. As a consequence, deducing personality from measures realized earlier in a subject's life should be performed with caution. We discuss the implications of inter‐ and intraindividual variation in personality consistency on individual fitness.     

Relationship between DHA status at birth and child problem behaviour at 7 years of age

Animal studies have demonstrated behavioural effects of long-chain polyunsaturated fatty acid (LC-PUFA) deficiencies and in humans, several psychiatric disorders have been linked to abnormal essential fatty acid metabolism. The aim of this study was to examine the relationship between LC-PUFA status at birth and the later development of problem behaviour. In a sample of 393 children, higher levels of docosahexaenoic acid (DHA) at birth were associated with lower levels of internalising problem behaviour at age 7 years. The association was markedly present in the infants fed with artificial formula (n=215, Beta=-0.32, P=0.000), but absent in the infants fed with human milk (n=170, Beta=0.11, P=0.325). The associations between arachidonic acid and internalising or externalising behaviour were neither large nor significant. The results suggest that perinatal DHA status may have long-term behavioural consequences. Therefore, we suggest to include measures of problem behaviour in future trials of LC-PUFA supplementation of mothers and/or infants.     

Behavioural Profiles in Captive-Bred Cynomolgus Macaques: Towards Monkey Models of Mental Disorders?

Background

To date, experimental and preclinical studies on neuropsychiatric conditions have almost exclusively been performed in experimentally-induced animal models and have only rarely relied upon an ethological approach where animals have been observed in more naturalistic settings. The laboratory species of choice has been the rodent while the potential of more closely-related non-human primates have remained largely underexplored.

Methods

The present study, therefore, aimed at investigating the possible existence of spontaneous atypical/abnormal behaviours displayed by 40 cynomolgus macaques in captive conditions using an unbiased ethological scan-sampling analysis followed by multifactorial correspondence analysis and a hierarchical clustering.

Results

The study identified five distinct profiles (groups A to E) that significantly differed on several behaviours, body postures, body orientations, gaze directions and locations in the cage environment. We suggest that animals from the low n groups (D and E) present depressive-like and anxious-like symptoms, reminiscent of depressive and generalized anxiety disorders. Inter-individual differences were highlighted through unbiased ethological observations of spontaneous behaviours and associated parameters, although these were not associated with differences in plasma or cerebrospinal fluid levels of either stress-related hormones or monoamines, i.e. in accordance with the human situation.

Conclusions

No interventional behavioural testing was required to discriminate between 3 typical and 2 atypical ethologically-defined behavioural profiles, reminiscent of certain depressive-like and anxiety-like symptoms. The use of unbiased behavioural observations might, thus, allow the identification of animal models of human mental/behavioural disorders and their most appropriate control groups.     

Imaging implicit perception: promise and pitfalls

The study of implicit perception - perception in the absence of awareness - has a long history. Decades of behavioural work have identified crucial theoretical and methodological issues that must be considered when evaluating claims of implicit perception. Neuroimaging methods provide an important new avenue for illuminating our understanding of perception both with and without awareness, but most imaging experiments have not met the rigorous conditions that the behavioural work has shown are necessary for inferring implicit perception. Here, we review the literature of both behavioural and neuroimaging studies, and note the pitfalls of studying implicit perception as well as the promise that neuroimaging studies have for providing insights about implicit perception when combined with appropriately rigorous behavioural measures of awareness.     

What we talk about when we talk about access deficits

Semantic impairments have been divided into storage deficits, in which the semantic representations themselves are damaged, and access deficits, in which the representations are intact but access to them is impaired. The behavioural phenomena that have been associated with access deficits include sensitivity to cueing, sensitivity to presentation rate, performance inconsistency, negative serial position effects, sensitivity to number and strength of competitors, semantic blocking effects, disordered selection between strong and weak competitors, correlation between semantic deficits and executive function deficits and reduced word frequency effects. Four general accounts have been proposed for different subsets of these phenomena: abnormal refractoriness, too much activation, impaired competitive selection and deficits of semantic control. A combination of abnormal refractoriness and impaired competitive selection can account for most of the behavioural phenomena, but there remain several open questions. In particular, it remains unclear whether access deficits represent a single syndrome, a syndrome with multiple subtypes or a variable collection of phenomena, whether the underlying deficit is domain-general or domain-specific, whether it is owing to disorders of inhibition, activation or selection, and the nature of the connection (if any) between access phenomena in aphasia and in neurologically intact controls. Computational models offer a promising approach to answering these questions.     

How do fish ectoparasites Argulus spp. (Crustacea: Branchiura) match with their hosts at the behavioural and ecological scales?

Features of the Argulus foliaceus and A. coregoni life cycles including spatial distribution and hatching patterns of the resting eggs as well as their host searching behaviour were analyzed on the basis of field and experimental data obtained in lakes and a fish farm in the Central Finland. Published data on behaviour and ecology of these parasites were also used. The main point of this analysis was an ecological adjustment of the life cycles of parasites to that of their fish hosts at different spatial and temporal scales. Due to different spatial distribution of overwintering eggs, the newly hatched larvae of A. coregoni are more likely to attach to salmonids, which are their main hosts, while A. foliaceus to percids and cyprinids. The main peak of argulid hatching occurs in late spring-early summer and coincides with the period when most of freshwater fishes concentrate close to the shore, either for spawning, or, foraging. Nevertheless, despite the general coincidence, the parasite-host encounter rate could still be very low. The main peak of hatching is followed by a long "tail". We suggest that under fluctuating and uncertain environmental conditions characterised by both abiotic stochasticity and poor predictability of the hosts, an optimal recruitment strategy is to hedge a bet, with a proportion of eggs synchronously hatching and a proportion remaining dormant and hatching at much lower rate during an extended period. One of the main behavioural adaptations to match with the hosts is all-over-the-day searching activity of argulids. The boreal A. coregoni relies primarily on vision, which is most effective in transparent waters during long polar days in summer. Vision is also important in the behavioural repertoire of the temperate A. foliaceus in the light, but olfaction and mechanoreception in the dark provide the highest host searching rate. The two generally sympatric species of argulids segregated on the finer habitat scale. Partially overlapping on salmonid hosts, they prefer ecologically distinct categories of fish, and use different microhabitats for egg laying and searching for hosts.     

Reproductive behaviour indicates specificity in resource use: phylogenetic examples from temperate and tropical insects

Specificity (= the degree of ecological specialisation) is one of the fundamental concepts of the science of ecology. Ambiguities on how to define and measure specificity have however complicated respective research efforts. Here we propose that, in insects, a behavioural trait – adult oviposition latency in captivity without a favourable host plant – correlates with a species’ specificity in larval host use. In the absence of a suitable host, monophagous insects are expected to wait for a long time before commencing oviposition, with the long waiting time corresponding to careful host location behaviour in nature. Polyphagous insects, in contrast, should be selected for an increased oviposition rate at the expense of the quality of oviposition substrate encountered and will on average have a short latency time. Using experimentally derived data on oviposition latency, we performed a phylogenetically informed analysis based on Bayesian inference to show that this variable correlates with host specificity (larval diet breadth) in a sample of north European species of geometrid moths. A closely related index – the probability to lay any eggs on an unfavourable substrate – shows an analogous pattern. To provide an example of how these indices can be applied, we compare our sample of geometrid moths from northern Europe with a sample from equatorial Africa. A comparative analysis based on an original phylogenetic reconstruction found no differences between the two study sites in parameters of oviposition behaviour. We conclude that behavioural tests can provide information about ecological interactions when the latter can not be directly recorded. Our example study also hints at the possibility that host specificity of herbivores is not necessarily higher in a tropical region compared to a temperate one.     

Behaviour of West Greenland caribou during a population decline

The major decline of the West Greenland caribou herd during the 1970s prompted a study in 1977–78 of caribou behaviour in relation to environmental factors associated with the decline. Quantification of caribou activity revealed behavioural responses to critically low standing crops of preferred winter forage. Caribou on poor winter range were mostly inactive with low feeding intensities and abnormal diurnal activity patterns. In addition, these animals exhibited very restricted movements, frequently occurred alone or in small groups, and were unable to maintain normal social bonds. In contrast, where fruticose lichen winter forage was available, caribou did not display these behavioural traits. After the initiation of new vegetative growth, feeding intensity increased and social tendency returned. Comparison with behavioural data from other Rangifer populations suggests that the observed responses to low forage quality are not restricted to Greenland but are a normal response of barren-ground caribou to winter ranges poor in lichen forage.     

Wanting,liking and welfare: The role of affective states in proximate control of behaviour in vertebrates

Animals choose a course of action countless times each day. To do so, they need to prioritise their behaviour within a set of alternative actions and decide which of these actions to perform at any one time and for how long, that is, determine when the behaviour has reached its desired effect. This process has classically been called the proximate behavioural control mechanism. Several aspects contribute to this process: internal and external stimuli, the emotions that they elicit, motivation (wants), behavioural goals, valuation, decision‐making and its modulation by mood, and the assessment of behavioural outcomes (liking). I will address all these aspects in the form of an integrated conceptual model. In the process of behavioural control, options need to be valued, and I will refer to evidence showing that an affective hedonic process in respect to (future) reward and punishment heavily affects this value. Moreover, I view motivation, the force that finally drives a specific behavioural output, as being primarily influenced by affective states or even corresponding fully to them. Given the feedback in behavioural control by (dis‐)liking outcomes of behaviour, I reason that in respect to welfare it is more important for animals to reach proximate goals than to avoid negative stimuli. All behavioural choices are modulated, and I show how mood, a long‐term affective state, can cause such modulation. Proximate control of behaviour takes place in the brain, and I will briefly discuss how current and future brain research may elucidate how the brain computes these processes. Furthermore, the inclusion of affective states in the conceptual model raises the question of the subjective experience of animals, and I will address some of the important open questions in this area of research. I will conclude that neural studies cannot currently provide a detailed and general theory on the algorithms of proximate behavioural control. In parallel to further developing these approaches, I propose to strengthen a refined ethological approach with a focus on the states of “wanting” and “liking” in ecologically meaningful circumstances and with a strong ontogenetic (within species) and comparative (between species) component. I consider this ethological approach to be a highly promising step in understanding proximate behavioural control.     

A spontaneous derivative of abnormal chromosome 10 in maize

Summary A new type of abnormal chromosome 10 has been found among maize plants grown from seeds sent by Dr. Y. C. Ting of Harvard University. This chromosome deviates in its morphology from the orthodox abnormal chromosome 10 described by Rhoades (1952) and from the one described by Ting (1958b). It produces a low degree of neo-centric activity.Cytological observations of plants heterozygous for the new abnormal chromosome 10 and either an orthodox abnormal chromosome 10 or a normal one, have suggested that the new type was derived from an orthodox abnormal 10 through spontaneous breakage and loss of an important piece of its long arm. The delection involved the distal part of the long arm of orthodox abnormal chromosome 10, proximally limited by the third most distal dissimilar and prominent chromomere. This corresponds approximately to the extra segment at the end of orthodox abnormal chromosome 10 which remains unpaired in heterozygotes with the normal 10. It bears a large heterochromatic knob. The missing piece is a part of the larger fraction of the long arm of orthodox abnormal chromosome 10 that remains unaffected by crossingover in a heteromorphic bivalent having a normal chromosome 10 (telo-segment). The telo-segment has its proximal limit at the left of the most proximal of the 3 dissimilar chromomeres, probably between the R and Sr ₂ loci. It has been proposed that a factor or factors responsible for neo-centric activity are located in the portion of the telosegment between its proximal limit and the third most distal dissimilar chromomere (3 dissimilar chromomere region).Since the telo-segment of the orthodox abnormal 10 also bears a large knob in its distal half, it has been suggested that this segment has a dual role in neo-centric activity. The factor or factors located in the proximal piece of the telo-segment would stimulate over-abundance of fiber-forming substance, whereas local production of chromosomal fibers would depend ultimately on the knob's activity.If the large knob is absent, its role in neo-centric activity would be transferred to the next smaller and distally located hetero-chromatic mass, such as the knob-like body near the end of the new abnormal 10 which results from the fusion of the two most proximal prominent chromomeres of the telo-segment.This work has been partly done in the United States, under an I.C.A. — National Academy of Sciences fellowship.     

Behavioural and endocrine fear responses in Japanese quail upon presentation of a novel object in the home cage

Most tests used to study fear in birds involve transferring them to a novel environment, which constitutes a bias in studies aiming at identifying the neural correlates of a specific fear-inducing situation. In order to investigate fear in birds with minimum interference by humans, behavioural and endocrine responses to the presentation of a novel object in the home cage were investigated in two lines of Japanese quail divergently selected for long or short duration of tonic immobility, a behavioural index of fear. Presentation of the novel object induced typical fear responses (avoidance of the object, increased pacing and increased plasma corticosterone levels) that were similar in the two lines of quail. Presentation of a novel object in the home cage thus appears to be a suitable stimulus to induce fear reactions in quail, with minimum interference from other motivational systems. The fact that quail of both lines reacted similarly in this test, while they are known to differ greatly in their behavioural responses to other fear-inducing tests, illustrates the multidimensional nature of fear.     

Behavioural Phenotyping of APPswe/PS1δE9 Mice: Age-Rrelated Changes and Effect of Long-Term Paroxetine Treatment

Alzheimer’s disease (AD) is a devastating illness characterized by a progressive loss of cognitive, social, and emotional functions, including memory impairments and more global cognitive deficits. Clinical-epidemiological evidence suggests that neuropsychiatric symptoms precede the onset of cognitive symptoms both in humans with early and late onset AD. The behavioural profile promoted by the AD pathology is believed to associate with degeneration of the serotonergic system. Using the APP_swe/PS1_δE9 model of AD-like pathology starting with 9 months old mice, we characterised long term non-cognitive behavioural changes measured at 9, 12, 15, and 18 months of age and applied principal component analysis on data obtained from open field, elevated plus maze, and social interaction tests. Long-term treatment with the selective serotonin reuptake inhibitor (SSRI) paroxetine was applied to assess the role of 5-HT on the behavioural profile; duration of treatment was 9 months, initiated when mice were 9 months of age. Treatment with paroxetine delays the decline in locomotion, in exploration and risk assessment behaviour, found in the APP/PS1 mice. APP/PS1 mice also exhibit low social activity and less aggressiveness, both of which are not affected by treatment with paroxetine. The APP/PS1 behavioural phenotype, demonstrated in this study, only begins to manifest itself from 12 months of age. Our results indicate that treatment with SSRI might ameliorate some of the behavioural deficits found in aged APP/PS1 mice.     

The behavioural state in human perinatal life

Behavioural states are easy to recognise in healthy neonates with a gestational age of 36 weeks or more. In younger neonates stable behavioural states, as seen at full-term, are not present, but activity cycles exist. In utero stable behavioural states can also be recognised from 36 to 38 weeks onwards. The existence of awake states in utero remains controversial. A close relationship exists between neural mechanisms regulating the behavioural state cycling and those modulating breathing. Our understanding of these is still very limited. The absence of behavioural states or of activity cycles is a very sensitive but non-specific sign of nervous system dysfunction in human perinatal life.     

Morphological and anatomical observations of abnormal somatic embryos from anther cultures of <Emphasis Type="Italic">Citrus reticulata</Emphasis>

A morphological and anatomical study of regenerants obtained from mandarin anther culture was carried out. Beside morphologically normal somatic embryos, abnormal structures were originated in the course of somatic embryogenesis. Anatomical anomalies can be found at several growth stages, causing the formation of slender stems, stubby structures, non-functional leaves. When too long, some structures are subject to shedding, with the formation of various abscission zones. Most of them are subject to degeneration, although many are capable of further, localized, morphogenesis. A thorough knowledge of morphology and anatomy of normal and abnormal regenerants could make possible to select and subculture the lines considered most suitable for conversion into plantlets.