Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella)

Numerous studies investigating behavioral lateralization in capuchins have been published. Although some research groups have reported a population-level hand preference, other researchers have argued that capuchins do not show hand preference at the population level. As task complexity influences the expression of handedness in other primate species, the purpose of this study was to collect hand preference data across a variety of high- and low-level tasks to evaluate how task complexity influences the expression of hand preference in capuchins. We tested eleven captive brown capuchin monkeys (Cebus apella) to determine if they show consistent hand preferences across multiple high- and low-level tasks. Capuchins were expected to display high intertask consistency across the high-level tasks but not the low-level tasks. Although most individuals showed significant hand preferences for each task, only two of the high-level tasks that involved similar hand motions were significantly positively correlated, indicating consistency of hand preference across these tasks only. None of the tasks elicited a group-level hand preference. High-level tasks elicited a greater strength of hand preference than did low-level tasks. No sex differences were found for the direction or strength of hand preference for any task. These results contribute to the growing database of primate laterality and provide additional evidence that capuchins do not display group-level hand preferences.     

Behavioural asymmetry affects escape performance in a teleost fish

Escape performance is fundamental for survival in fish and most other animals. While previous work has shown that both intrinsic (e.g. size, shape) and extrinsic (e.g. temperature, hypoxia) factors can affect escape performance, the possibility that behavioural asymmetry may affect timing and locomotor performance in startled fish is largely unexplored. Numerous studies have found a relationship between brain lateralization and performance in several cognitive tasks. Here, we tested the hypothesis that behavioural lateralization may affect escape performance in a teleost, the shiner perch Cymatogaster aggregata. Escape responses were elicited by mechanical stimulation and recorded using high-speed video (250 Hz). A number of performance variables were analysed, including directionality, escape latency, turning rate and distance travelled within a fixed time. A lateralization index was obtained by testing the turning preference of each subject in a detour test. While lateralization had no effect on escape directionality, strongly lateralized fish showed higher escape reactivity, i.e. shorter latencies, which were associated with higher turning rates and longer distances travelled. Therefore, lateralization is likely to result in superior ability to escape from predator attacks, since previous work has shown that escape timing, turning rate and distance travelled are among the main determinants of escape success.     

Chicken or egg? Outcomes of experimental manipulations of maternally transmitted hormones depend on administration method – a meta‐analysis

Steroid hormones are important mediators of prenatal maternal effects in animals. Despite a growing number of studies involving experimental manipulation of these hormones, little is known about the impact of methodological differences among experiments on the final results expressed as offspring traits. Using a meta‐analytical approach and a representative sample of experimental studies performed on birds, we tested the effect of two types of direct hormonal manipulations: manipulation of females (either by implantation of hormone pellets or injection of hormonal solutions) and manipulation of eggs by injection. In both types of manipulation we looked at the effects of two groups of hormones: corticosterone and androgens in the form of testosterone and androstenedione. We found that the average effect on offspring traits differed between the manipulation types, with a well‐supported positive effect of egg manipulation and lack of a significant effect of maternal manipulation. The observed average positive effect for egg manipulation was driven mainly by androgen manipulations, while corticosterone manipulations exerted no overall effect, regardless of manipulation type. Detailed analyses revealed effects of varying size and direction depending on the specific offspring traits; e.g., egg manipulation positively affected physiology and behaviour (androgens), and negatively affected future reproduction (corticosterone). Effect size was negatively related to the dose of androgen injected into the eggs, but unrelated to timing of manipulation, offspring developmental stage at the time of measuring their traits, solvent type, the site of egg injection and maternal hormone delivery method. Despite the generally acknowledged importance of maternal hormones for offspring development in birds, the overall effect of their experimental elevation is rather weak, significantly heterogeneous and dependent on the hormone and type of manipulation. We conclude by providing general recommendations as to how hormonal manipulations should be performed in order to standardize their impact and the results achieved. We also emphasize the need for research on free‐living birds with a focus on fitness‐related and other long‐term effects of maternal hormones.     

Eggshell Spottiness Reflects Maternally Transferred Antibodies in Blue Tits

Blue-green and brown-spotted eggshells in birds have been proposed as sexual signals of female physiological condition and egg quality, reflecting maternal investment in the egg. Testing this hypothesis requires linking eggshell coloration to egg content, which is lacking for brown protoporphyrin-based pigmentation. As protoporphyrins can induce oxidative stress, and a large amount in eggshells should indicate either high female and egg quality if it reflects the female''s high oxidative tolerance, or conversely poor quality if it reflects female physiological stress. Different studies supported either predictions but are difficult to compare given the methodological differences in eggshell-spottiness measurements. Using the blue tit Cyanistes caeruleus as a model species, we aimed at disentangling both predictions in testing if brown-spotted eggshell could reflect the quality of maternal investment in antibodies and carotenoids in the egg, and at improving between-study comparisons in correlating several common measurements of eggshell coloration (spectral and digital measures, spotted surface, pigmentation indices). We found that these color variables were weakly correlated highlighting the need for comparable quantitative measurements between studies and for multivariate regressions incorporating several eggshell-color characteristics. When evaluating the potential signaling function of brown-spotted eggshells, we thus searched for the brown eggshell-color variables that best predicted the maternal transfer of antibodies and carotenoids to egg yolks. We also tested the effects of several parental traits and breeding parameters potentially affecting this transfer. While eggshell coloration did not relate to yolk carotenoids, the eggs with larger and less evenly-distributed spots had higher antibody concentrations, suggesting that both the quantity and distribution of brown pigments reflected the transfer of maternal immune compounds in egg yolks. As yolk antibody concentrations were also positively related to key proxies of maternal quality (egg volume, number, yellow feather brightness, tarsus length), eggshells with larger spots concentrated at their broad pole may indicate higher-quality eggs.     

Lateralization in the predatory behaviour of the common wall lizard (Podarcis muralis)

Ectotherms have been shown being lateralized as well as mammals and birds. This is particularly evident in visual lateralization, i.e. the different use of the eyes, leading to use a specific eye to observe specific kind of stimuli and to process them with the correspondent contralateral hemisphere. Several lower vertebrates are facilitated in this from the lateral position of the eyes, enabling them to carry out more tasks simultaneously, controlled by different eyes and relative hemispheres. Predatory responses seem usually mediated by the right eye/left hemisphere in fishes, amphibians and some sauropsids, but there are no strong evidences of this in lizards. Eighteen wild males of the Common wall lizard Podarcis muralis were tested individually in captivity to ascertain whether they are lateralized to look at prey with a specific eye. The lizards were gently induced entering a 30-cm long central arm of a T-maze which led to a 44.5-cm long arm cross-arm at whose extremities there were two identical prey, Tenebrio molitor larvae, familiar to the lizards. We recorded what direction the lizards chose to reach the prey and the frequency and duration of head turning, indicative of looking either prey with the left or the right eye. We found that individuals show being lateralized at individual level. The preferred direction taken to reach the prey is the right for the majority of those (4 of 5) showing an evident preference, indicating also a possible form of laterality at population level. In addition, lizards maintained the same head side of the direction taken turned for more time towards the prey than the opposite head side, revealing an eye preference for observing this kind of cue. Our study demonstrates how males of Podarcis muralis have a visual lateralization to capture prey. Furthermore, it is another support to the hypothesis of vertebrate lateralization derivation from a common ancestor.     

Influence of mate preference and laying order on maternal allocation in a monogamous parrot species with extreme hatching asynchrony

It is well established that in many avian species, prenatal maternal resource allocation varies both between and within clutches and may affect offspring fitness. Differential allocation of maternal resources, in terms of egg weight and yolk composition, may therefore allow the female to adjust brood reduction and to fine-tune reproductive investment in accordance with the expected fitness returns. The adaptive value of such maternal resource allocation is thought to be context-dependent as well as species-specific. We investigated the effects of female preference for her mate on the allocation of prenatal maternal resources in the budgerigar, Melopsittacus undulatus, a monogamous species of parrot that shows an extreme hatching asynchrony. We assessed mate preferences in a two-way preference test and allowed females two breeding rounds: one with the preferred and one with the non-preferred partner. We found no effect of preference on either latency to lay or clutch size, but females mated with the preferred partner laid eggs that contained significantly more yolk. Their eggs also contained significantly more androstenedione but not testosterone. Our results suggest that in this species, female preference may influence maternal resource allocation, and that the functional roles of each androgen in the yolk should be considered separately. In addition, we found a significant effect of laying order on egg and yolk weight as well as on yolk testosterone and androstenedione levels. These measures, however, did not change linearly with the laying order and render it unlikely that female budgerigars compensate for the extreme hatching asynchrony by adjusting within-clutch allocation of prenatal maternal resources.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Individual Consistency and Phenotypic Plasticity in Rockhopper Penguins: Female but Not Male Body Mass Links Environmental Conditions to Reproductive Investment

In marine habitats, increasing ocean temperatures due to global climate change may distinctly reduce nutrient and consequently food availability for seabirds. Food availability is a known driver of body mass and reproductive investment in birds, but these traits may also depend on individual effects. Penguins show extreme intra-annual body mass variation and rely on accumulated body reserves for successful breeding. However, no study so far has tested individual consistency and phenotypic responses in body mass and reproductive investment in this taxon. Using a unique dataset on individually marked female and male southern rockhopper penguins (Eudyptes chrysocome chrysocome) across six years, we investigated 1) the individual consistency in body mass (measured at egg laying), body condition and reproductive investment across years, subsequently 2) identified the best-explanatory temperature-related environmental variables for female and male body mass, and 3) tested the effect of female and male body mass on reproductive investment. Body mass, body condition and reproductive investment were all highly repeatable. As body condition should control for the structural size of the birds, the similarly high repeatability estimates for body mass and body condition suggested that the consistent between-individual body mass differences were independent of structural size. This supported the use of body mass for the subsequent analyses. Body mass was higher under colder environmental conditions (positive Southern Annular Mode), but the overall phenotypic response appeared limited. Reproductive investment increased with female but not male body mass. While environmental effects on body mass in our study period were rather small, one can expect that ongoing global climate change will lead to a deterioration of food availability and we might therefore in the long-term expect a phenotypical decline in body mass and reproductive investment.     

Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds

Recent studies on hormone-mediated maternal effects in birds have highlighted the influence of variable maternal yolk androgen concentration on offspring phenotype, particularly in terms of early development. If genetic differences between laying females regulate variation in yolk hormone concentration, then this physiological maternal effect is an indirect genetic effect which can provide a basis for the co-evolution of maternal and offspring phenotypes. Thus, we investigated the evolutionary associations between maternally derived yolk testosterone (T) and early developmental traits in passerine birds via a comparative, phylogenetic analysis. Our results from species-correlation and independent contrasts analyses provide convergent evidence for the correlated evolution of maternal yolk T concentration and length of the prenatal developmental period in passerines. Here, we show these traits are significantly negatively associated (species-correlation: p<0.001, r2=0.85; independent contrasts: p=0.005). Our results highlight the need for more studies investigating the role of yolk hormones in evolutionary processes concerning maternal effects.     

The effect of maternal state on the steroid and macronutrient content of lesser black-backed gull eggs

It has been proposed that female birds can influence the phenotype of their offspring by provisioning eggs with variable amounts of nutrients and maternal hormones. Egg quality is strongly influenced by maternal body reserves and the amount of food available at the time of egg formation. This study investigated the effects of maternal state and food availability on the capacity of female lesser black-backed gulls Larus fuscus to provision their eggs with macronutrients and steroid hormones. Maternal state was reduced by increasing egg-production effort, whereas extra food was provided to reverse this effect. Compared with eggs of first clutches, eggs of experimentally induced replacement clutches exhibited a lower yolk/albumen ratio and contained more yolk testosterone. During one of the three years in which the study was performed, replacement eggs also contained more 17β-estradiol. Food provisioning during the relaying interval did not affect changes in yolk/albumen ratio or steroid concentrations, but fed females produced bigger eggs in their replacement clutch. This study demonstrates significant within-female consistency in egg size, macronutrient content, and yolk steroid concentration, and it shows that these egg characteristics are influenced by maternal state, food availability, and the timing of breeding.     

Carotenoids and egg quality in the lesser blackbacked gull Larus fuscus: a supplemental feeding study of maternal effects.

Egg quality is a phenotype of, and can profoundly influence fitness in, both mother and offspring. However, the physiological mechanisms that underlie this maternal effect are poorly understood. Carotenoids are hypothesized to enhance antioxidant activity and immune function, and are responsible for the pigmentation of egg yolk. The proximate basis and consequences of this maternal investment, however, have not previously been studied in wild birds. In this supplemental feeding study of lesser black-backed gulls, Larus fuscus, carotenoid-fed females are shown to have increased integument pigmentation, higher plasma concentrations of carotenoids and antioxidant activity, and lower plasma concentrations of immunoglobulins (Igs) in comparison with controls. In turn, carotenoid-fed females produced eggs containing high carotenoid but low Ig concentrations (i.e. passive immunity), whereas control females produced eggs containing low carotenoid but high Ig concentrations. Within-clutch patterns of these resources varied over the laying sequence in a similar manner in both carotenoid-fed and control nests. Our results suggest that carotenoids could be one resource responsible for egg quality maternal effects in birds. We discuss the possible implications of carotenoid-mediated effects on phenotype for fitness in mothers and their offspring.     

Elevated plasma corticosterone decreases yolk testosterone and progesterone in chickens: linking maternal stress and hormone-mediated maternal effects

Despite considerable research on hormone-mediated maternal effects in birds, the underlying physiology remains poorly understood. This study investigated a potential regulation mechanism for differential accumulation of gonadal hormones in bird eggs. Across vertebrates, glucocorticoids can suppress reproduction by downregulating gonadal hormones. Using the chicken as a model species, we therefore tested whether elevated levels of plasma corticosterone in female birds influence the production of gonadal steroids by the ovarian follicles and thus the amount of reproductive hormones in the egg yolk. Adult laying hens of two different strains (ISA brown and white Leghorn) were implanted subcutaneously with corticosterone pellets that elevated plasma corticosterone concentrations over a period of nine days. Steroid hormones were subsequently quantified in plasma and yolk. Corticosterone-implanted hens of both strains had lower plasma progesterone and testosterone levels and their yolks contained less progesterone and testosterone. The treatment also reduced egg and yolk mass. Plasma estrogen concentrations decreased in white Leghorns only whereas in both strains yolk estrogens were unaffected. Our results demonstrate for the first time that maternal plasma corticosterone levels influence reproductive hormone concentrations in the yolk. Maternal corticosterone could therefore mediate environmentally induced changes in yolk gonadal hormone concentrations. In addition, stressful situations experienced by the bird mother might affect the offspring via reduced amounts of reproductive hormones present in the egg as well as available nutrients for the embryo.     

Development of Lateralization of Unconditional Motor Reactions in Early Ontogenesis of White Rats

The problem of development of lateralization of motor systems in the course of early ontogenesis is important for understanding regularities of formation of functional characteristics of motor control. To solve these tasks, in the 8–74-day old rat pups the presence of lateralization was studied in two motor tests: the choice of the preferable rotation direction at holding the rat by the tail and the choice of one of the forelimbs in the test of initiation of the limb placement onto a support. It has been shown that in early ontogenesis, until the age of the sexual maturation, no constant lateralization is observed in realization of the unconditional motor reactions in any of the performed tests. The turning point of the establishment of the lateral preference has been revealed to correspond to the three-week age (the 21–23rd days), while the final lateralization both for individual animals and for the entire sample takes place at the age of 1.5–2 months. It is suggested that development of lateralization of the limb placement on a support occurs with the approximately two-week delay as compared with the process of formation of the preference in the choice of the rotation direction.     

A behavioral analysis of prey detection lateralization and unilateral transfer in European starlings (Sturnus vulgaris)

It has been suggested that birds prefer to use a particular eye while learning to detect cryptic prey and that this eye preference enhances foraging performance. European starlings (Sturnus vulgaris) with the left, right, or both eyes available learned to detect inconspicuous cues associated with the presence of hidden prey. Acquisition scores were not significantly different between left and right-eyed birds; however, performance in the binocular condition was significantly higher than in the two monocular conditions. When binocular birds were tested with familiar and unfamiliar cues present simultaneously, the familiar cue was selected significantly more often than the unfamiliar cue, suggesting that the birds were searching for specific cue features. When monocular birds were tested using only the naïve eye, performance dropped significantly. In right-eyed birds using the naïve left eye, performance remained at chance levels over transfer trials. However, left-eyed birds using the naïve right eye had a superior performance compared to the initial acquisition scores of right-eyed birds and also showed a significant improvement in performance over transfer trials. Thus, although there was no direct evidence of lateralization during acquisition, there was unilateral transfer of the prey detection skill from the right to the left hemisphere.     

Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus

In birds, experimentally increased egg production can reduce maternal condition, parenting ability and survival, and the quality of the eggs themselves. Such costs probably reflect resource limitation, but the identity of the resource(s) in question remains unclear. Carotenoids are antioxidants and immunomodulants that birds can only obtain in their diet. Trade-offs in the allocation of limiting carotenoids between somatic maintenance and egg production could therefore be an important factor underlying reproductive costs. We show that in wild lesser black-backed gulls, Larus fuscus, dietary carotenoid availability (i) constrained the capacity to re-lay following clutch removal; and (ii) affected the relationship between yolk mass and egg mass. However, whether carotenoids are limiting for egg production directly, by stimulating the synthesis or antioxidant protection of yolk precursors, or indirectly via effects on maternal health, requires further study.     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

Patterns of hand and mouth lateral biases in bamboo leaf shoot feeding and simple food reaching in the gentle lemur (Hapalemur griseus)

Lateralized feeding behaviors of 7 wild-born and 6 captive-born Hapalemur griseus sp. were evaluated in two conditions, simple food reaching and species-typical bamboo foraging. Gentle lemurs were found to have the strongest lateral hand preference in simple food reaching of any prosimian species yet studied. However in this small sample, population-level lateralization was not found: 5 preferred the right hand and 8 the left. The movement pattern used by hapalemurs when feeding on bamboo leaf shoots was categorized into four components: PULL IN, COUNTERFORCE, TURN, and FEED IN. Lateral hand bias was scored for all four components and lateral mouth preference was scored for the two components that involved the mouth (COUNTERFORCE and FEED IN). Strong positive correlations were found between hand preference in the most lateralized components of shoot eating (TURN and FEED IN) and simple food reaching. This suggests that the gentle lemurs' species-typical bamboo feeding behavior may contribute to the exceptionally strong hand preference for simple food reaching seen in this species. There were negative correlations between the component measure of shoot feeding that required strength (COUNTERFORCE) and the components that required manipulation (TURN and FEED IN). Within the COUNTERFORCE and FEED IN components, mouth preference and hand preference were positively associated in a manner that suggested one side of the mouth was preferred for removing the shoot and the other side for mastication. Asymmetrical dental wear may provide a means of dating behavioral lateralization in ancestral species. © 1993 Wiley-Liss, Inc.     

The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models

Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and/or among clutches. Here we tested for such correlations between maternally derived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed-model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed-model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology.     

Lateral asymmetry of eye use in Octopus vulgaris

The lateralization of sensory and motor functions has been recently demonstrated in various groups of vertebrates. We examined lateral asymmetry of eye use in Octopus vulgaris by behavioural methods. Octopus vulgaris uses monocular vision almost exclusively and can move its eyes independently. The amount of binocular vision is small because the eyes are on the sides of the head. We tested eight octopuses in two conditions (one with and one without moving stimuli) where the use of the eye for frontal vision could be determined unequivocally. Data were recorded on videotape. All animals showed a preference for one eye (five left, three right). There was no correlation between eye use and the animal's direction of movement. Pigmentation of the ventral side of the arms tended to be most intense on the side of the preferred eye and the body was most pigmented on the side of the eye currently in use. We found no sex differences for visual lateralization. Pigmentation of the ventral side of the arms was lighter in females than in males. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Maternal effects and offspring performance: in search of the best method

Traditionally, maternal effects have been treated as a source of troublesome environmental variance that confounds our ability to accurately estimate the genetic basis of the traits of interest. However, the adaptive significance of maternal effects is currently at the centre of the attention of ecologists. Thus, in turn, the genetic basis of traits has become a troublesome source of the genetic resemblance that confounds our ability to accurately estimate the maternal effects of interest. This fact is, however, less widely realized among ecologists. We demonstrate this on the example of studies investigating egg-size effects on offspring performance in birds. Traditionally this relationship is being studied by cross-fostering of eggs or young and it is claimed that this design is able to separate the effects of egg size per se. However, a positive covariation between the direct effects of genes and the maternal effects exists for many studied traits, which may result in overestimation of the egg-size effects on offspring performance in cross-fostering studies. Within-clutch comparisons or direct experimental manipulation of the egg size are the approaches that do not suffer from such covariation and therefore give less biased estimates of the egg-size effects than cross-fostering studies.