Attachment security in companion dogs: adaptation of Ainsworth's strange situation and classification procedures to dogs and their human caregivers.

This exploratory study describes the development of a classification system for dogs' attachment security to caregivers that adheres closely to Ainsworth's seminal methodology. Fifty-nine adult dogs and caregivers participated in a mildly threatening laboratory encounter with a stranger (TS) and the Strange Situation (SSP). Dog and attachment experts adapted Ainsworth's classification system  for the behavioral repertoire of the dog. Four potentially comparable patterns of attachment were identified. The proportions of secure and insecure classifications (61% and 39%) were similar to those found in human toddlers. Caregivers' sensitivity to their dogs during the TS procedure significantly differentiated dogs with secure vs. insecure classifications Lower scores on the Active/excited personality scale on the Monash Canine Personality Questionnaire-Revised (MCPQ-R) also were related to secure classification. This system now makes it possible to compare directly the effects of human and dog attachment patterns on the health and emotional well-being of humans and dogs.

Female androgen patterns and within-pair testosterone compatibility in domestic geese (Anser domesticus).

For successfully raising offspring, long-term monogamous pair partners need to be behaviorally and hormonally coordinated. In the monogamous, biparental greylag geese (Anser anser) a dyadic pairbond-specific measure, 'within-pair testosterone compatibility' (TC) indicated how closely synchronized are seasonal androgen levels, which co-varied with reproductive output. Males, in particular, were assumed to respond to their females' hormonal and fecundity phases. We now present experiments with biparental domestic geese (Anser domesticus) kept as pairs to ask whether TC occurs also in these generally polygynous animals. We further ask how different conditions of mate choice affect TC and whether established TC is maintained during a polygynous flock situation. We measured androgen metabolites (AM) non-invasively from individual droppings. In females, AM was related with gonadal activity as it increased after GnRH but not ACTH challenge. Females with preferred partners had higher maximum AM during egg laying and higher rates of initiating incubation than randomly paired females. Domestic ganders had seasonal AM patterns typical for polygynous males. Within-pair TC ranged from almost perfectly positive to non-correlated in domestic geese but mate choice did not explain TC variation. TC of previous pairs was generally reduced in the flock situation, probably confounded by factors of the social environment, i.e. mating opportunity and availability of multiple partners. On top of the underlying reproductive physiology our results suggest two episodic components of TC: a female androgen responsiveness to the preferred partner at least during egg formation, and the male's facultative potential to respond to her readiness to breed.

Individual and sex differences in learning abilities of ravens.

Behavioral and physiological characteristics of individuals within the same species have been found to be stable across time and contexts. In this study, we investigated individual differences in learning abilities and object and social manipulation to test for consistency within individuals across different tasks. Individual ravens (Corvus corax) were tested in simple color and position discrimination tasks to establish their learning abilities. We found that males were significantly better in the acquisition of the first discrimination task and the object manipulation task, but not in any of the other tasks. Furthermore, faster learners engaged less often in manipulations of conspecifics and exploration of objects to get access to food. No relationship between object and social manipulation and reversal training were found. Our results suggest that individual differences in regard to the acquisition of new tasks may be related to personalities or at least object manipulation in ravens.

Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica).

The yolk of avian eggs contains steroid hormones, which may influence the development and behaviour of hatched birds. The aim of the present study was to investigate the concentration as well as the distribution of various gonadal steroids in the yolk spheres of quail eggs. Steroid concentrations of dissected yolk layers were analysed after alcoholic extraction using enzyme immunoassays (EIAs) for progesterone, androstenedione and testosterone. To monitor the uptake of testosterone into the yolk, radioactive testosterone was injected i.m. into six female quails. The radioactivity of yolk layers of subsequently laid eggs was measured by liquid scintillation counting. Progesterone concentrations were highest in the outer layer (median: 2265 nmol/kg). Androstenedione (median: 453 nmol/kg), as the major androgen, and testosterone (median: 99 nmol/kg) reached their highest concentrations in interior layers, whereas in the centre the concentration of all three hormones was low. No significant variation of steroid levels in yolk layers of subsequently laid eggs was found. The highest radioactivity was detected in the outer yolk layer in those eggs laid 1 day after injection and in subsequently laid eggs was measured nearer to the centre. These results indicated local origin of the steroid hormones especially because of the result that only 0.1% of the radioactivity entered the yolk. We conclude that steroid concentrations in the yolk layers reflected progesterone and androgen production of the cells of the follicular wall at the time.

Excreted metabolites of gonadal steroid hormones and corticosterone in greylag geese (Anser anser) from hatching to fledging.

Steroid hormones play major roles in the organization of the phenotype and in the activation of behavior. From hatching to fledging, they are involved in growth, development, and learning. We investigated the relationship between the ontogenetic patterns of steroid hormones and the sexual and social development of greylag goslings (Anser anser). Two groups of individually marked goslings (n = 10/5) were hand-raised under near-field conditions. 17beta-OH-androgen (AM), estrogen (EM), and corticosterone (BM) immunoreactive metabolites were measured noninvasively by enzyme immunoassay of individual fecal samples. Feces were regularly sampled from hatching to fledging. All excreted steroids were found to peak at hatching and to decrease thereafter. Gonadal steroids fluctuated more than BM, which remained at low levels throughout ontogeny after a slow decrease during the first 20 days. The pattern of BM is discussed in relation to learning processes (i.e., filial imprinting) and social stress. It is suggested that high initial BM may constrain energy allocation to growth. AM increased around the age of 20 days, when the feathers start growing, and later, together with EM, at the age of 40 days. These elevated values of gonadal steroids are discussed in relation to the sensitive phase of sexual imprinting. Females show higher EM levels than males throughout ontogeny. Furthermore, the ratio of excreted estrogen to androgen (EM/AM) of females before fledging correlates with the number of hatched and fledged goslings in their first years of reproduction. In conclusion, our data suggest a role for steroid hormones in the modulation of behavioral and morphological development in the precocial greylag geese, in agreement with the organizational-activational hypothesis.

Seasonal relationships between plasma and fecal testosterone in response to GnRH in domestic ganders.

In two groups (eight individuals each) of socially acquainted, outdoor-kept, domestic ganders (male Hungarian white: Anser domesticus), basal and GnRH-stimulated plasma testosterone (T) concentrations were compared with fecal testosterone metabolites (TM) in and between three seasons, spring peak of reproductive activity, summer photorefractoriness, and fall sexual reactivation. Plasma was sampled 90 min following the challenge and T was analyzed by radioimmunoassay following the GnRH challenge. Fecal TM were measured by enzyme immunoassay using two group-specific antibodies against 17beta-OH-androgens or a novel antibody against 17-oxo groups, which was found to react with major testosterone metabolites without prior hydrolytic deconjugation. Baseline plasma T and systemic levels were high in spring and fall but low in summer. Plasma T increases in response to GnRH were followed by significantly elevated fecal TM levels 2 to 6 h following the challenge in spring and fall. In fall, at high plasma T levels, fecal TM levels were disproportionally lower than in spring. Variability of TM levels was two to five times higher in feces than in plasma, which explains why correlations between individual plasma T and fecal TM levels generally remained nonsignificant. This points to a low-level short-term relationship between the excreted TM and the plasma T levels. However, the reliability of the method was demonstrated by standard inter- and intraassay variabilities and by a high correspondence between results obtained by the two assays. It is suggested that, with appropriate sample size, fecal TM reflects plasma T increase. However, fecal TM was more variable than the plasma T, and fecal TM responses to GnRH did not always parallel the plasma T response. In addition, seasonal changes in androgen excretion regimes must be taken into account.

Stimulus enhancement in greylag geese: socially mediated learning of an operant task.

We recently observed the spreading of a novel tradition in a flock of semiferal greylag geese, Anser anser: an increasing number of individuals began to bite and chew the stems of butterbur, Petasites hybridus. Because this behaviour spread particularly fast within families, social learning seemed to be involved. We therefore designed an experiment with hand-reared goslings, which were socially imprinted on humans, to investigate whether and how the observation of an experienced tutor affects the acquisition of a novel skill. Goslings had to open the gliding lid of a box to get at a food reward. To each of seven hand-reared observers a human tutor demonstrated where and how to open the lid, whereas seven controls remained untutored. All observers learned to perform the task but only one of the controls succeeded. The observers explored more often at the position shown by the tutor than elsewhere and seemingly learned by trial and error. In contrast, control birds explored primarily at positions that did not allow them to open the box. These results indicate that in greylag goslings the observation of an experienced model facilitates the learning of an operant task. We conclude that stimulus enhancement followed by operant conditioning were the mechanisms involved, which may have accounted for the fast spread of the stem-chewing tradition between family members. Copyright 2000 The Association for the Study of Animal Behaviour.

Taste(s) and olfaction(s) in fish: a review of specialized sub-systems and central integration.

Evidence from comparative morphology and electrophysiology suggests that both, olfaction and taste in fish serve different ecological roles. The lateral olfactory system (dorsolateral olfactory bulb glomeruli and lateral olfactory tract) and the external taste buds are probably specialized for food search and amino acid discrimination. The medial olfactory system (basomedial olfactory bulb glomeruli and medial olfactory tract) and the solitary chemosensory taste cells, however, may have their roles in intra- and interspecific interactions (discriminating pheromones by olfaction, bile components by both olfaction and taste). Whereas stimulation of the taste systems alone triggers reflexes, complex, conditional or conditioned behaviours are only released when the olfactory system is intact. This points at the importance of telencephalic and diencephalic integration of olfactory and taste inputs. Consequently, caution is appropriate concerning simplistic interpretations of deprivation experiments.

Social learning in common ravens, Corvus corax.

We conducted an experiment to investigate whether the presence of a conspecific model can promote the acquisition of a motor task in common ravens. For this purpose, dyads, either of control birds or of model-observer pairings, were allowed to operate together in an arena with a set of identical boxes. Each box consisted of two compartments each containing a reward of three pieces of meat. The compartments were closed by gliding lids with red flaps on their front, opening horizontally in opposite directions. Naive control individuals opened the lids exclusively by levering, that is, jumping on top of the box, inserting the beak at the posterior rim of the lid and pushing it open. Models were trained to demonstrate an alternative opening technique, pulling at the front flap, then jumping on top of the box to get at the reward. In contrast to the control birds, observers initially opened boxes both ways, by pulling and levering. Furthermore, observers approached the boxes more quickly and showed less fearful behaviour than the control birds, which we attribute to the enhancing effect of the model. We discuss both stimulus enhancement and motor imitation as possible learning mechanisms. Even though observers initially obtained a considerable amount of reward produced by the models, scrounging evidently did not inhibit learning. Copyright 1999 The Association for the Study of Animal Behaviour.

Seasonal patterns of sex steroids determined from feces in different social categories of Greylag geese (Anser anser).

Seasonal patterns of fecal 17beta-OH-androgen, estrogen, and progesterone equivalents of male and female greylag geese (Anser anser) were analyzed in a flock of free-living geese. These were compared among social categories determined by pairbond status and breeding success. The annual cycle was divided into 13 phases. Phasewise intra-sexual comparisons were made between social categories. The seasonal variation obtained from feces was in general agreement with the literature on plasma patterns in geese and other temperate-zone birds. However, there were distinct differences in seasonal hormone patterns among the social categories. In unpaired males, androgen was elevated for a longer period of time during sexually active phases compared with paired males. In male geese, high levels of androgen did not interfere with parenting but were related to pairbond status, whereas in females, androgen and progesterone were positively related to parental behavior. In the Fall, androgen, progesterone, and estrogen peaked only in unpaired males. In unsuccessful females, estrogen started to increase earlier in the Winter and was higher in amplitude and duration than that in females guarding offspring. In general, fecal steroids showed a clear-cut difference only between sexually active and parental phases of the year in the successfully breeding pairs, whereas unpaired males retained a hormonal state closer to sexually active phases throughout the year.

The relationship between social stress and dominance is seasonal in greylag geese

Studies of captive animals have suggested that social stress affects subdominants, whereas recent data from the wild have revealed that stress mainly affects dominants. We used a non-invasive approach to investigate, for the first time in a social bird, the circannual stress-dominance relationships between low-ranking single males, intermediately positioned paired ganders without offspring and high-ranking paired males with offspring from a flock of semi-tame, free-ranging greylag geese, Anser anser. We collected 933 faecal samples from 43 individuals, 12 singletons, 18 paired males without offspring and 13 paired males with offspring over an entire year and analysed them for corticosterone metabolites by enzyme immunoassay. During the mating season (February-April), singletons had marginally higher corticosterone than paired males (P<0.1), whereas during the parental season (May-January), the paired males with offspring had significantly higher corticosterone than both paired males without offspring and singletons. All three male categories had significantly higher corticosterone during the mating season than during the rest of the year. These results suggest that social stress in ganders is caused mainly by competition between males and by constrained access to females during the mating season, but by parental commitment during the rest of the year. We suggest that dominance per se may not be a direct cause of stress. Rather, the amount of social stress may co-vary with the behavioural investment individuals need to make to optimize their fitness and with the relationship between such demands and the individuals' rank positions. This relationship seems to be seasonal in geese. Copyright 1998 The Association for the Study of Animal Behaviour.

High-voltage electron microscopy and 3-D reconstruction of solitary chemosensory cells in the anterior dorsal fin of the Gadid fish Ciliata mustela (Teleostei).

Solitary chemosensory cells (SCCs) are secondary sensory cells present in the epidermis of most primary aquatic vertebrates. In rocklings, the epidermis of the anterior dorsal fin (ADF) contains approximately 5 million SCCs. High-voltage electron microscopy and three-dimensional reconstructions from serial sections were used to examine the ultrastructure, arrangement, and synaptic contacts of the SCCs in the rockling ADF. Approximately 15% of all cells in the fin ray epidermis are SCCs, which occupy roughly 30% of the epidermal volume. These spindle-shaped cells are 25-30 microm long and up to 10 microm wide and terminate apically in a microvillus protruding 2-5 microm above the epidermal surface. SCCs contain abundant endoplasmic reticulum and a large Golgi apparatus in their proximal regions. The distal parts of SCCs contain characteristic vesicles, elongate mitochondria, and longitudinal strands of intermediate filaments. Synapses between SCCs and nerves resemble those found in teleost taste buds. One to four synaptic contacts per SCC were found. We hypothesize that the apparent secretory activity of the SCCs serves to replenish the apical membrane and mucus. Furthermore, parallel sampling of several hundred SCCs by single nerve fibers may serve low-threshold detection rather than stimulus localization.

Ontogeny of the solitary chemosensory cells in the zebrafish, Danio rerio.

Secondary epidermal solitary chemosensory cells (SCCs) are widespread among the primary aquatic vertebrates. They resemble taste bud sensory cells in fine structure and may be innervated from facial or spinal nerves. According to previous studies, SCCs may constitute a water sampling system in the contexts of predator avoidance, habitat recognition and, in some cases, finding food. By quantitative scanning (SEM) and transmission electron microscopy (TEM) in 60 specimens (57 SEM, 3 TEM) of 16 developmental stages, from pre-hatchlings to adults, we describe the ontogenetic development of SCC densities and shapes of sensory apices in the zebrafish, Danio rerio. This is put into perspective with the ontogeny of external taste buds. Just prior to hatching, 3 days after fertilization (3d AF), sensory apices of SCCs penetrate between the squamous epidermal cells, whereas taste bud pores only appear at the onset of exogenous feeding (5d AF). SCC densities increase sharply from hatching shortly after metamorphosis (25d AF) up to 6 x 10(3) per mm2 on the head and remain relatively constant in density thereafter. Conservatively estimated, there may be approximately 3.2 x 10(5) SCCs on the head and 1 x 10(6) SCCs on the entire body surfaces of a zebrafish 180d AF. SCCs are spread evenly, but are 2- to 5-fold higher in density along the head than along the body. Sensory apices are brush-like in hatchlings and early juveniles, but tend to consist of a single villus in the adults. This ontogenetic change of SCC apices parallels the evolutionary change from 'oligovillous' cells in lampreys and elasmobranchs to the 'monovillous' SCCs in the advanced actinopterygian teleosts.

Secondary connections of the dorsal and ventral facial lobes in a teleost fish, the rockling (Ciliata mustela).

In the rockling, Ciliata mustela (Teleostei), a portion of the dorsal fin is a specialized chemosensory organ possessing solitary chemoreceptor cells innervated by a recurrent branch of the facial nerve. Previous studies have demonstrated that the specialized solitary chemoreceptor cell system is represented in the dorsal segment of the medullary facial lobe (DFL), whereas the taste buds in the remainder of the facial-nerve-innervated skin are represented in the ventral division of the lobe (VFL). The carbocyanine dye DiI was used to investigate the secondary and higher order brain connections of these two distinct subdivisions of the facial lobe. Both segments of the facial lobe sent fibers into the contralateral DFL via a dorsocaudal facial commissure and to the contralateral vagal lobes and VFL via fibers arching ventrally through the reticular formation. Ascending fibers from both facial lobe segments were traced into the secondary gustatory nucleus and into the lateral superficial facial nucleus, a small area in the dorsolateral brainstem laterally adjacent to the nucleus medialis of the octavolateral complex. Additionally, the VFL had reciprocal connections with a newly described nucleus adjacent to the incoming facial nerve root. Both DFL and VFL had descending fibers reaching two portions of the funicular nuclear complex, although the VFL contribution to this area is far more extensive than the DFL input. Thus, substantial overlap exists in the connections of the two facial subsystems; i.e., the solitary chemoreceptor information is not processed in nuclei distinct from those making up the usual gustatory lemniscus.

Solitary chemosensory cells: why do primary aquatic vertebrates need another taste system?

The taste-like system of solitary chemosensory cells (SCCs) has almost eluded scientific attention. This is particularly remarkable, since recent surveys have revealed that this system of epidermal cells is widespread and abundant among the anamniotic aquatic vertebrates. In the rocklings (Gadidae, Teleostei), high densities of SCCs occur at a specialized dorsal fin. Recent evidence from this model indicates that SCCs are narrowly tuned to dilutions of fish body mucus and bile. Thus, SCCs may sample the ambient water for the upstream presence of potential competitors or predators. However, in sea robins (Triglidae, Teleostei), SCCs seem to be involved in finding food. Information from many more species is needed to explain why SCCs and taste buds have been maintained in parallel for such a long evolutionary period of time - from the age of the agnathans to that of the most advanced teleost fishes.

Spinal and facial innervation of the skin in the gadid fish Ciliata mustela (Teleostei).

The pattern of innervation of the skin of the rockling Ciliata mustela was investigated to sort out spinal from facial nerve innervation of cutaneous chemosensory and mechanosensory systems. This fish has a variety of appendages with different functional sensory specializations, i.e., the chin barbel, pelvic fin, anterior dorsal fin, and dorsal trunk skin. The carbocyanine dye, diI, was applied to nerve stumps in dissected aldehyde-fixed tissue. In the case of the chin barbel, the dye was applied to both the trigeminal and facial nerve components. In the other cases, the dye was applied either selectively to the spinal nerves, to the facial nerves, or to both components. In the chin barbel, diI labeled nerve fibers associated with taste buds (TBs) and solitary chemosensory cells (SCCs) as well as relatively blunt free nerve endings, which closely approach the epidermal surface. In the pelvic fin, anterior dorsal fin, and dorsal trunk skin, taste buds, solitary chemosensory cells, and their innervation were labeled only after diI was applied to the facial nerve stumps. Application of diI to spinal nerves labeled delicate, free nerve endings and nerve fibers associated with small cells deep in the epidermis with features characteristic of Merkel cells. Transmission electron microscopy supports these results; after denervation of the facial component of the anterior dorsal fin, synaptic contacts with Merkel cells remained intact, whereas the synapses with the SCCs vanished.

Postlarval growth of the peripheral gustatory system in the channel catfish, Ictalurus punctatus.

The phenomenon of postlarval cell addition to the peripheral nervous system of fish has been reported for some sensory systems, but has yet to be characterized for the gustatory system. Many fishes, such as catfish, possess taste buds scattered across their body surface, and presumably, the number of taste buds increases during growth of the animal. The present study was undertaken in order to examine the process of growth in the peripheral gustatory system and to determine whether the degree of convergence of receptors onto primary sensory afferents changes during growth. The recurrent facial nerve of channel catfish was used for these studies since this nerve contains no general cutaneous components and innervates taste buds along the fish's body surface. Electron micrographs were made of cross sections of this nerve taken from individuals ranging in size from 5.1 to 39.5 cm standard length. In addition, estimates were made of the number of taste buds innervated by this nerve by determining taste bud density along selected regions of the flank and fins in large and small fish. As catfish get larger, the number of both myelinated and unmyelinated axon profiles in the recurrent facial nerve increases, but at a slower rate than the number of taste buds innervated by this nerve. Thus, on average, the number of taste buds innervated by each fiber increases as the fish enlarges; on average there are 2 taste buds per axons profile in small fish and nearly 14 taste buds per axon profile in large fish. The rate of addition of new axon profiles to the nerve is estimated at roughly 70 per day over the range of sizes studied. Although generation of new ganglion cells and axons may contribute to this increase, several lines of evidence indicate that axonal branching occurs. In addition, the mean axon diameter for both myelinated and unmyelinated axons increases during postlarval growth. The finest myelinated fibers (0.2 micron) in small animals were significantly smaller than the finest myelinated fibers (0.7 micron) in larger animals.

Retinal morphology of cyprinid fishes: a quantitative histological study of ontogenetic changes and interspecific variation.

Morphological patterns of the retina, cone size and density, rod density, rod-cone ratio, ganglion cell density, convergence of receptor cells, resolving power (RP) and regionalization were examined throughout life history in roach and in adults of asp, bream, common carp, roach and sabre carp. The retina of hatchlings is packed with small cones. During larval and juvenile growth the retina stretches, cones increase in diameter and rods are present in increasing numbers. Photopic and scotopic sensitivity as well as resolving power increase. Comparison of adults shows distinct interspecific differences in retinal parameters, which can be related to life style.

Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus).

This study compares brain growth in 4 species of cyprinids, each distinctly different in adult brain morphology: roach have generalized brains; bream are characterized by well-developed visual, octavolateralis and gustatory brain regions; common carp show chemosensory (gustatory)-dominated brains, and sabre carp octavolateralis-dominated brains. The growth patterns of 16 regions relative to total brain volume were investigated by computer-aided quantitative histology to illustrate internal brain allometries. In all species the tectum opticum decreases in relative size during growth, whereas the corpus cerebelli increases. In bream and common carp, primary taste centers steadily increase in relative size during growth. In most if not all fish, the brain attains no definite final morphology. Lifelong, growth-related shifts in relative sizes of primary sensory regions may reflect lifelong shifting sensory capabilities.

Life history of roach, Rutilus rutilus (Cyprinidae, Teleostei). A qualitative and quantitative study on the development of sensory brain areas.

The present study deals with aspects of the brain development in the roach, Rutilus rutilus, a common mid-European cyprinid fish. The morphogenesis of selected brain areas from hatching to early juveniles was examined on serial paraffin cross-sections. From early juveniles to large adults, brain growth was quantitatively analyzed by computer-aided planimetry. The hatchlings of roach show a cytologically distinct optic tectum, but a poorly differentiated brainstem, reflecting the predominance of the optic sense during the larval planktivorous period. The differentiation and outgrowth of chemosensory brainstem centers is related to the onset and development of benthivorous feeding in juveniles. The optic tectum decreases in size relative to the total brain volume from juveniles through adults. The corpus cerebelli increases in relative size, whereas chemosensory and acousticolateral centers grow isometrically with the brain as a whole.