Dynamics of Bacterial Communities on Eggshells and on Nest Materials During Incubation in the Oriental Tit (Parus minor).

Eggshell bacterial communities may affect hatching success and nestling's condition. Nest materials are in direct contact with the eggshells, but the relationships with the eggshell microbiome during incubation have not been fully elucidated. Here, we characterize eggshell and nest material bacterial communities and their changes during incubation in the Oriental Tit (Parus minor). Bacterial communities on the nest material were relatively stable and remained distinct from the eggshell communities and had higher diversity and greater phylogenetic clustering than the eggshell communities from the same nest, resulting in lower phylogenetic turnover rate of nest material microbiome during incubation than expected by chance. While the species diversity of both communities did not change during incubation, we found significantly greater changes in the structure of bacterial communities on the eggshell than on the nest material. However, eggshell microbiome remained distinct from nest material microbiome, suggesting independent dynamics of the two microbiomes during incubation. We detected an increase in the relative abundance of several bacterial taxa on the eggshell that likely come from the bird's skin, feathers, cloaca/intestine, or uropygial secretion which suggests some exchange of bacteria between the incubating bird and the eggshell. Furthermore, incubation appeared to promote the abundance of antibiotic producing taxa on the eggshell, which may hypothetically inhibit growth of many bacteria including pathogenic ones. Our results suggest that the future studies should focus on simultaneous monitoring of absolute abundance as well as relative abundance in communities on eggshells, nest materials, and the incubating bird's body.

Association between host wing morphology polymorphism and Wolbachia infection in Vollenhovia emeryi (Hymenoptera: Myrmicinae).

Many eusocial insects, including ants, show complex colony structures, distributions, and reproductive strategies. In the ant Vollenhovia emeryi Wheeler (Hymenoptera: Myrmicinae), queens and males are produced clonally, while sterile workers arise sexually, unlike other ant species and Hymenopteran insects in general. Furthermore, there is a wing length polymorphism in the queen caste. Despite its evolutionary remarkable traits, little is known about the population structure of this ant species, which may provide insight into its unique reproductive mode and polymorphic traits. We performed in-depth analyses of ant populations from Korea, Japan, and North America using three mitochondrial genes (COI, COII, and Cytb). The long-winged (L) morph is predominant in Korean populations, and the short-winged (S) morph is very rare. Interestingly, all L morphs were infected with Wolbachia, while all Korean S morphs lacked Wolbachia, demonstrating a association between a symbiont and a phenotypic trait. A phylogenetic analysis revealed that the S morph is derived from the L morph. We propose that the S morph is associated with potential resistance to Wolbachia infection and that Wolbachia infection does not influence clonal reproduction (as is the case in other ant species).

Visual stimulation-induced mild stress enhances cognitive behavior in cynomolgus monkey.

Cortisol is a well-known endogenous glucocorticoid that serves as a stress indicator. It is normally released under stressful condition to warn about imminent danger and thus is critical for survival of the species. However, it is unclear how cortisol relates to cognitive process under physiological condition in high-order primates such as non-human primates (NHP). Here, we report that a slight but significant increase in blood cortisol level by mild stress is positively correlated with the cognitive function in cynomolgus monkey. We stimulated 3 groups of monkeys by viewing consecutive series of pictures of monkeys, pictures of humans, or animation still pictures. We first found that the blood cortisol level was significantly higher during the stimulation session and returned to normal after stimulation session. Among the three types of pictures, the monkeys which were stimulated with monkey pictures showed the most significant increase in cortisol level during stimulation. Furthermore, the monkeys showed significantly enhanced manipulation, suggesting that cortisol affected cognitive processes. Overall, our study demonstrates that visual stimulation both increases blood cortisol and enhances manipulating behavior. Therefore, unlike the common notion that cortisol is a stress indicator, our data supports that a mild increase of cortisol enhances cognition in NHP.

Microbial abundance on the eggs of a passerine bird and related fitness consequences between urban and rural habitats.

Urban environments present novel and challenging habitats to wildlife. In addition to well-known difference in abiotic factors between rural and urban environments, the biotic environment, including microbial fauna, may also differ significantly. In this study, we aimed to compare the change in microbial abundance on eggshells during incubation between urban and rural populations of a passerine bird, the Eurasian Magpie (Pica pica), and examine the consequences of any differences in microbial abundances in terms of hatching success and nestling survival. Using real-time PCR, we quantified the abundances of total bacteria, Escherichia coli/Shigella spp., surfactin-producing Bacillus spp. and Candida albicans on the eggshells of magpies. We found that urban magpie eggs harboured greater abundances of E. coli/Shigella spp. and C. albicans before incubation than rural magpie eggs. During incubation, there was an increase in the total bacterial load, but a decrease in C. albicans on urban eggs relative to rural eggs. Rural eggs showed a greater increase in E. coli/Shigella spp. relative to their urban counterpart. Hatching success of the brood was generally lower in urban than rural population. Nestling survival was differentially related with the eggshell microbial abundance between urban and rural populations, which was speculated to be the result of the difference in the strength of the interaction among the microbes. This is the first demonstration that avian clutches in urban and rural populations differ in eggshell microbial abundance, which can be further related to the difference in hatching success and nestling survival in these two types of environments. We suggest that future studies on the eggshell microbes should investigate the interaction among the microbes, because the incubation and/or environmental factors such as urbanization or climate condition can influence the dynamic interactions among the microbes on the eggshells which can further determine the breeding success of the parents.

Orangutans (Pongo spp.) do not spontaneously share benefits with familiar conspecifics in a choice paradigm.

Humans are thought to be unique in their ability to help others voluntarily even though it may sometimes incur substantial costs. However, there are a growing number of studies showing that prosocial behaviors can be observed, not only in humans, but also among nonhuman primates that live in complex social groups. Prosociality has often been described as a major factor that facilitates group living. Nonetheless, it has seldom been explored whether solitary living primates, such as orangutans, share this propensity. In the present study, we tested four captive orangutans (Pongo abelii × pigmaeus, Pongo pigmaeus) in a simple food-delivering task. They had a choice, incurring the same cost, between getting a food reward for themselves and providing an additional food reward to a conspecific recipient passively sitting in an adjacent booth. Two orangutans played the actor's role, and two orangutans participated as recipients. The results showed that the actors did not choose to deliver food to the recipients more often than expected by chance (51.3 % on average). The control condition demonstrated that this tendency was independent of the actor's understanding of the task. These findings suggest that orangutans do not spontaneously share benefits with other conspecifics, even when the prosocial choice does not disadvantage them. This study gives the first experimental evidence that socially housed captive orangutans do not behave prosocially in a choice paradigm experiment. Further studies using a different experimental paradigm should be conducted to examine whether this tendency is consistent with previous findings hypothesizing that the enhanced prosocial propensity shown in humans and other group living primates is an evolutionary outcome of living in complex social environments.

Effect of incubation on bacterial communities of eggshells in a temperate bird, the Eurasian Magpie (Pica pica).

Inhibitory effect of incubation on microbial growth has extensively been studied in wild bird populations using culture-based methods and conflicting results exist on whether incubation selectively affects the growth of microbes on the egg surface. In this study, we employed culture-independent methods, quantitative PCR and 16S rRNA gene pyrosequencing, to elucidate the effect of incubation on the bacterial abundance and bacterial community composition on the eggshells of the Eurasian Magpie (Pica pica). We found that total bacterial abundance increased and diversity decreased on incubated eggs while there were no changes on non-incubated eggs. Interestingly, Gram-positive Bacillus, which include mostly harmless species, became dominant and genus Pseudomonas, which include opportunistic avian egg pathogens, were significantly reduced after incubation. These results suggest that avian incubation in temperate regions may promote the growth of harmless (or benevolent) bacteria and suppress the growth of pathogenic bacterial taxa and consequently reduce the diversity of microbes on the egg surface. We hypothesize that this may occur due to difference in sensitivity to dehydration on the egg surface among microbes, combined with the introduction of Bacillus from bird feathers and due to the presence of antibiotics that certain bacteria produce.

Changes in fecal estrogen levels and sexual behavior in captive sichuan snub-nosed monkeys (Rhinopithecus roxellana) following a male replacement.

Rhinopithecus roxellana are generally seasonal breeders, although copulation can occur throughout the year. Previous studies suggest that estradiol modulates female sexual behavior during the mating season. However, the effects of social context on estrogen levels and behavior have not been fully explored. We studied the relationship between sexual behaviors and fecal estrogens in a group of captive R. roxellana during a period of social instability. We collected behavioral data for six months and collected fecal samples at 2-3-day intervals for four months spanning the mating and nonmating seasons, and analyzed fecal estrogen levels via RIA. Females showed clear cyclic solicitation and copulation peaks in the mating season, which corresponded with sharp peaks in fecal estrogens. During the nonmating season, solicitation rates, copulation rates, and fecal estrogens were generally low. However, one nonpregnant female displayed a sharp peak in solicitations, copulations, and estrogens during the nonmating season 10-14 days after a male replacement. Our results provide preliminary evidence that social and behavioral changes affect estrogen levels in R. roxellana.

Genetic composition of communal roosts of the Eurasian Magpie (Pica pica) inferred from non-invasive samples.

Many animal species form communal roosts in which they aggregate and sleep together. Several benefits of communal roost have been suggested, but due to lack of data on relatedness among group members, it is unknown whether these benefits can be amplified by the formation of kin-based communal roosts. We investigate the genetic composition of two winter roosts of Eurasian Magpies (Pica pica), using microsatellite markers on non-invasive samples. Using permutation tests by reshuffling the alleles presented in the roosts, we determined that individuals in the communal roosts of magpies were not more related than expected by chance, suggesting that kinship may not be a driving force for the formation of communal roosts in magpies. However, the pairwise relatedness and estimated relationship based on a maximum likelihood approach revealed that the roosts involve both kin and non-kin. Relatedness coefficients varied widely within a roost, indicating that family subgroups form a small proportion of the total number of birds in a roost. Our results suggest that ecological benefits of communal roost in animals are sufficient for the evolution of communal roosts without any involvement of kinship.

Comparative phylogeography of two widespread magpies: importance of habitat preference and breeding behavior on genetic structure in China.

Historical geological events and climatic changes are believed to have played important roles in shaping the current distribution of species. However, sympatric species may have responded in different ways to such climatic fluctuations. Here we compared genetic structures of two corvid species, the Azure-winged Magpie Cyanopica cyanus and the Eurasian Magpie Pica pica, both widespread but with different habitat dependence and some aspects of breeding behavior. Three mitochondrial genes and two nuclear introns were used to examine their co-distributed populations in East China and the Iberian Peninsula. Both species showed deep divergences between these two regions that were dated to the late Pliocene/early Pleistocene. In the East Chinese clade of C. cyanus, populations were subdivided between Northeast China and Central China, probably since the early to mid-Pleistocene, and the Central subclade showed a significant pattern of isolation by distance. In contrast, no genetic structure was found in the East China populations of P. pica. We suggest that the different patterns in the two species are at least partly explained by ecological differences between them, especially in habitat preference and perhaps also breeding behavior. These dissimilarities in life history traits might have affected the dispersal and survival abilities of these two species differently during environmental fluctuations.

Low resolution of mitochondrial COI barcodes for identifying species of the genus Larus (Charadriiformes: Laridae).

We evaluated whether cytochrome c oxidase subunit I (COI) barcodes that have been previously suggested for birds are useful for identifying species of the genus Larus, which are resident or migratory birds in Korea. We found 31 intra- or interspecific COI haplotypes from 12 of 13 Larus species in Korea. Haplotype analyses showed that the COI barcodes could not distinguish some interspecific haplotypes from 6 of 12 Larus species because there were no nucleotide substitutions among their COI haplotypes. The neighbor-joining tree formed shallow branches in the clades expected for L. saundersi, L. crassirostris, L. canus, L relictus, and L. ridbundus. In the nine Larus species, COI haplotypes were not grouped as distinct entities that were correctly assigned to their corresponding species, resulting in polytypic clades. These results indicate that the COI sequences need to be cautiously selected as a DNA barcode for identifying species of Korean Larus birds.

Is female preference for large sexual ornaments due to a bias to escape predation risk?

BACKGROUND: A female preference for intense sexual visual signals is widespread in animals. Although the preferences for a signal per se and for the intensity of the signal were often regarded to have the identical origin, no study has demonstrated if this is true. It was suggested that the female fiddler crabs prefer males with courtship structures because of direct benefit to escape predation. Here we tested if female preference for both components (i.e. presence and size) of the courtship structure in Uca lactea is from the sensory bias to escape predation. If both components have the identical origin, females should show the same response to different-sized courtship structures regardless of predation risk. RESULTS: First, we observed responses of mate-searching female U. lactea to courting males with full-sized, half-sized and no semidomes which were experimentally manipulated. Females had a directional preference for males with bigger semidomes within normal variation. Thereafter, we tested the effect of predation risk on the female bias in the non-courtship context. When threatened by an avian mock predator, females preferentially approached burrows with full-sized semidomes regardless of reproductive cycles (i.e. reproductive periods and non-reproductive periods). When the predator cue was absent, however, females preferred burrows with semidomes without discriminating structure size during reproductive periods but did not show any bias during non-reproductive periods. CONCLUSIONS: Results indicate that selection for the size of courtship structures in U. lactea may have an origin in the function to reduce predation risk, but that the preference for males with structures may have evolved by female choice, independent of predation pressure.

Wild birds recognize individual humans: experiments on magpies, Pica pica.

The ability to distinguish among heterospecific individuals has been reported in only a few animal species. Humans can be viewed as a special type of heterospecifics because individuals differ widely in behavior, ranging from non-threatening to very threatening toward animals. In this study, we asked whether wild magpies can recognize individual humans who had accessed their nests. We compared the behavior of breeding pairs toward individual humans before and after the humans climbed up to the birds' nests, and also toward climbers and non-climbers. We have evidence for (i) aggressive responses of the magpie pairs toward humans who had repeatedly accessed their nests (climbers) and a lack of response to humans who had not accessed the nest (non-climbers); (ii) a total lack of scolding responses toward climbers by magpie pairs whose nests had not been accessed; (iii) a selective aggressive response to the climber when a climber and a non-climber were presented simultaneously. Taken together, these results suggest that wild magpies can distinguish individual humans that pose a threat to their nests from humans that have not behaved in a threatening way. The magpie is only the third avian species, along with crows and mockingbirds, in which recognition of individual humans has been documented in the wild. Here, we propose a new hypothesis (adopted from psychology) that frequent previous exposure to humans in urban habitats contributes to the ability of birds to discriminate among human individuals. This mechanism, along with high cognitive abilities, may predispose some species to learn to discriminate among human individuals. Experimental tests of these two mechanisms are proposed.

Convergent and divergent patterns of morphological differentiation provide more evidence for reproductive character displacement in a wood cricket Gryllus fultoni (Orthoptera: Gryllidae).

BACKGROUND: In ecological character displacement, traits involved in reproductive isolation may not evolve in arbitrary directions when changes in these traits are by-products of adaptation to an ecological niche. In reproductive character displacement, however, selection acts directly on reproductive characters to enhance the degree of reproductive isolation between sympatric populations. Thus, the direction of change in reproductive characters may be arbitrary in relation to changes in other morphological characters. We characterized both tegminal characters and characters indicative of body size in sympatric and allopatric populations of Gryllus fultoni, a species displaying character displacement in its calling song characters in areas of sympatry with G. vernalis populations, to infer the nature and direction of selection acting on reproductive and morphological characters in sympatry. RESULTS: Except for mirror area, the number of teeth in a file, and ovipositor length of G. fultoni, all male and female morphological characters in G. fultoni and G. vernalis exhibited a uniform tendency to decrease in size with increasing latitude. There was no significant variation in female morphological characters between sympatric and allopatric G. fultoni populations. However, males of sympatric and allopatric G. fultoni populations significantly differed in head width, hind femur length, and mirror area even after controlling for clinal factors. Head width and hind femur length of G. fultoni were more similar to those of G. vernalis in sympatric populations than in allopatric populations, resulting in morphological convergence of G. fultoni and G. vernalis in sympatry. However, the mirror area of G. fultoni displayed the divergent pattern in relation to the sympatric G. vernalis populations. CONCLUSION: Divergence-enhancing selection may be acting on mirror area as well as calling song characters, whereas local adaptation or clinal effects may explain variation in other morphological characters in sympatric populations of G. fultoni. This study also suggests that structures and behaviors that directly enhance reproductive isolation may evolve together, independently of other morphological traits.

Commensalism or mutualism: conditional outcomes in a branchiobdellid-crayfish symbiosis.

A growing body of evidence suggests that the costs and benefits involved in cleaning interactions can vary over space and time depending on the environmental conditions. However, whether the same cleaners actually induce variable net outcomes in terms of host fitness remains unclear to date. Branchiobdellid annelids are generally regarded as commensals or rarely parasites of their freshwater crayfish hosts, but a recent study suggests that they may also function as cleaning organisms. Under natural conditions, crayfish can experience fouling of the exposed surfaces of their exoskeletons and their gills (e.g., epibiosis) by various epibionts and particles of organic debris, and branchiobdellids graze on these sources of fouling. Here, we examined the extent to which variation in fouling pressure in the environment alters the outcome of the interaction between branchiobdellids and their crayfish host Cambaroide similis. A series of manipulations were performed in artificial environments designed to simulate either high or low fouling pressure. We used crayfish growth rates and mortality as direct measurements of the net costs and benefits of cleaning. Branchiobdellids had no significant effect on crayfish growth or mortality when cultured under low fouling pressure. However, their presence had a significant positive impact on host growth rates when cultured under high fouling pressure. These results suggest that the relationship between crayfish and branchiobdellids can fluctuate between commensalism and mutualism depending mainly on the environmental fouling pressure. We hypothesize that the outcome of cleaning interactions may largely depend on the factors directly related to the need for cleaning, such as parasite loads or fouling pressure.

Sex preferences in Jeju pony foals (Equus caballus) for mutual grooming and play-fighting behaviors.

We investigated mutual grooming by Jeju pony (Equus caballus) foals to determine whether male foals preferentially interact with potential future sexual partners or competitors. We predicted that relative to female foals, male foals would exchange grooming more frequently with young mares and that in general, foals would mutually groom more frequently with the opposite sex rather than the same sex. Observing 53 foals between April and October 1998, we recorded 113 mutual grooming events. Male foals exchanged grooming with yearling mares more frequently than with their mother, while female foals exchanged grooming with their mother more frequently than with yearling mares. Contrary to the prediction, foals were not more likely to mutually groom with a foal of the opposite sex than with a foal of the same sex. In our study, 21 instances of play-fighting behavior followed mutual grooming between peers. Relative to intersexual grooming events, play-fighting was more likely to follow intrasexual mutual grooming, and male foals were much more likely to play fight than female foals. These results provide evidence that Jeju pony foals develop and maintain social relationships at the earliest stage of their lives. We suggest that early social experiences might influence social bonding later when the male foal begins to form a harem after separation from its mother.

The postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation, and synaptic protein expression.

Many environmental factors during the pre- or postnatal period can affect an individual's cognitive function and neural development throughout life. Little is known, however, about the combined effects of the pre- and postnatal environments on cognitive function of adult offspring and structural alterations in the adult brain. In this study, we confirmed that pre- or postnatal stress impaired learning and memory performance of rats. Conversely, pre- or postnatal enriched housing improved behavioral performance. These experience-dependent behavioral alterations were consistent with changes in 5-bromo-2'-deoxyuridine-labeled cell number in the granule cell layer of the hippocampus and in the expression level of synaptic markers such as neuronal cell adhesion molecule and synaptophysin, and expression of a neurotrophic factor, brain-derived neurotrophic factor. Postnatal stress appeared to have no influence on cell proliferation, however. We did find that postnatal environment could attenuate prenatal effects partly via a longitudinal cross-housing study, in which pups born to mothers housed under enriched conditions were reared under stressful conditions and vice versa. These results suggest that postnatal environmental manipulations can counteract the cognitive alterations in early adulthood and the structural changes in the young adult brain induced by prenatal experience.

Reproductive skew and the origin of sterile castes.

Reproductive skew theory has not heretofore formally addressed one of the most important questions in evolutionary biology: How can whole-life sterile castes evolve? We construct a transactional skew model investigating under what conditions a subordinate in a multimember group is favored to develop into a morphologically specialized worker caste. Our model demonstrates that, contrary to former expectations, the ecological and genetic conditions favoring caste differentiation are far more restrictive than those favoring high skew. Caste differentiation cannot be selected in saturated, symmetrical relatedness groups unless the genetic relatedness among group members is extremely high. In contrast, it can be selected in the saturated, asymmetrical relatedness (parent-offspring) groups with complete skew. If we also consider the future reproduction of subordinates, caste differentiation is possible only after the group size reaches a certain critical point. Most importantly, caste differentiation in a parent-offspring group increases its saturated group size. The positive feedback between group size and the degree of caste differentiation can continue in principle until completely sterile worker castes emerge. Thus, at least in the case of parent-offspring groups, group size but not the degree of reproductive skew may be a better index of the level of social complexity. A scheme for the evolution of sterile worker castes that integrates the role of group size into the framework of reproductive skew theory is proposed.

Colony composition, social behavior and some ecological characteristics of the Korean wood-feeding cockroach (Cryptocercus kyebangensis).

Korean populations of the genus Cryptocercus occur in forested mountains throughout South Korea. They live in monogamous associations in which parents care for their young in complex woody galleries. Single paired adults (23.2%) and one or both parents with their offspring (28.1%) were found most frequently in the field. Among single-parent families adult females (6.7%) were observed more frequently than adult males (1.4%). In families with single or both parents, the mean brood size was 21.6+/-9.4. Oothecae were observed from mid-June to the late July. Oothecae were found in the galleries of only paired adults and never found in families with nymphs. The mean number of eggs per female was 73.7+/-29.8. Most of neonates grew to the third or fourth instar prior to the winter. During the winter, C. kyebangensis in the field remained almost frozen in their galleries, but ones kept in the laboratory continued to grow during winter. Some characteristics of proctodeal feeding behavior are also described based on laboratory observations. We propose that the cold temperate climate, especially of the winter season, is one of the most important causes for the evolution of unusual life history of Cryptocercus including delayed development of nymphs.