'Ripple effects' of urban environmental characteristics on cognitive performances in Eurasian red squirrels.

Urban areas are expanding exponentially, leading more species of wildlife living in urban environments. Urban environmental characteristics, such as human disturbance, induce stress for many wildlife and have been shown to affect some cognitive traits, such as innovative problem-solving performance. However, because different cognitive traits have common cognitive processes, it is possible that urban environmental characteristics may directly and indirectly affect related cognitive traits (the ripple effect hypothesis). We tested the ripple effect hypothesis in urban Eurasian red squirrels residing in 11 urban areas that had different urban environmental characteristics (direct human disturbance, indirect human disturbance, areas of green coverage and squirrel population size). These squirrels were innovators who had previously repeatedly solved a food extraction task (the original task). Here, we examined whether and how urban environmental characteristics would directly and indirectly influence performance in two related cognitive traits, generalisation and (long-term) memory. The generalisation task required the innovators to apply the learned successful solutions when solving a similar but novel problem. The memory task required them to recall the learned solution of the original task after an extended period of time. Some of the selected urban environmental characteristics directly influenced the task performance, both at the population level (site) and at individual levels. Urban environmental characteristics, such as increased direct and indirect human disturbance, decreased the proportion of success in solving the generalisation task or the memory task at the population (site) level. Increased direct human disturbance and less green coverage increased the solving efficiency at individual levels. We also found an indirect effect in one of the urban environmental characteristics, indirect human disturbance, in the generalisation task, but not the memory task. Such an effect was only seen at the individual level but not at the population level; indirect human disturbance decreased the first original latency, which then decreased the generalisation latency across successes. Our results partially support the ripple effect hypothesis, suggesting that urban environmental characteristics are stressors for squirrels and have a greater impact on shaping cognitive performance than previously shown. Together, these results provide a better understanding of cognitive traits that support wildlife in adapting to urban environments.

Consistent Negative Correlations between Parasite Infection and Host Body Condition Across Seasons Suggest Potential Harmful Impacts of Salmincola markewitschi on Wild White-Spotted Charr, Salvelinus leucomaenis.

Assessing the impacts of parasites on wild fish populations is a fundamental and challenging aspect of the study of host-parasite relationships. Salmincola, a genus of ectoparasitic copepods, mainly infects salmonid species. This genus, which is notorious in aquaculture, damages host fishes, but its impacts under natural conditions remain largely unknown or are often considered negligible. In this study, we investigated the potential impacts of mouth-attaching Salmincola markewitschi on white-spotted charr (Salvelinus leucomaenis) through intensive field surveys across four seasons using host body condition as an indicator of harmful effects. The prevalence and parasite abundance were highest in winter and gradually decreased in summer and autumn, which might be due to host breeding and/or wintering aggregations that help parasite transmissions. Despite seasonal differences in prevalence and parasite abundance, consistent negative correlations between parasite abundance and host body condition were observed across all seasons, indicating that the mouth-attaching copepods could reduce the body condition of the host fish. This provides field evidence suggesting that S. markewitschi has a potential negative impact on wild white-spotted charr.

Parasites either reduce or increase host vulnerability to fishing: a case study of a parasitic copepod and its salmonid host.

Parasites generally increase host vulnerability to predators via host manipulation for trophic transmission and reduction of host activities. Predators also select prey depending on the parasite infection status. Despite such parasites' roles in prey-predator interactions in wild animals, how parasites affect human hunting probability and resource consumption remains unknown. We examined the effects of the ectoparasitic copepod Salmincola cf. markewitschi on fish vulnerability to angling. We found that infected fish were less vulnerable compared with non-infected fish when the fish body condition was low, which was probably due to reduced foraging activity. On the contrary, infected fish were more vulnerable when the host body condition was high, probably due to the compensation of parasites' negative effects. A Twitter analysis also suggested that people avoided eating fish with parasites and that anglers' satisfaction decreased when captured fish were parasitized. Thus, we should consider how animal hunting is affected by parasites not only for catchability but also for avoiding parasite infection sources in many local regions.

A novel phylogenetic comparative method for evaluating the strength of branch-specific directional selection.

Phylogenetic comparative methods (PCMs) have played a central role in studying the evolution of phenotypic traits. However, when a trait experienced directional selection, previous PCMs have faced a dilemma between mathematically tractable but restrictive models (i.e., simple Gaussian process models) and flexible but intractable approaches (i.e., a simulation-based process model of phenotype evolution built on population genetics frameworks). This paper proposes a novel Gaussian process macroevolutionary model, called the "branch-specific directional selection (BSDS)," for evaluating the strength of directional selection to reconcile these two approaches. This model is based on a second-order approximation of a previous simulation-based process model but has a closed-form likelihood function. This can also be extended to incorporate intraspecies variations and to linear mixed models, which are necessary for meta-analysis. We conduct numerical experiments to validate the proposed method and apply it to the brain volume of Hominidae species. The results show that the proposed methods yield statistically more reliable inferences and computational time is about hundred thousand times faster than the previous simulation-based methods. Further extensions of the BSDS model are expected to provide a clearer picture of the connection of microevolutionary processes and macroevolutionary patterns.

Salmincola markewitschi or S. carpionis (Copepoda: Lernaeopodidae)? A requirement for taxonomic revision due to their high morphological variations.

Salmincola markewitschi Shedko et Shedko, 2002 (Copepoda: Lernaeopodidae) is an ectoparasitic copepod mainly infecting the buccal cavities of white-spotted charr Salvelinus leucomaenis (Pallas) (Salmonidae). This species has only been recorded from Northeast Asia, where a morphologically similar congener Salmincola carpionis (Krøyer, 1837) is also distributed, using the same host species. These copepods are hard to distinguish from each other because of their similarities. We thus examined the newly collected specimens morphologically and genetically from five populations of white-spotted charr in Japan. Most of the specimens were morphologically consistent with S. markewitschi but showed great variations in the numbers of spines on the exopods of the antennae, shape of the maxilliped myxal palps, and the bulla diameter. Consequently, some specimens shared characteristics with S. carpionis. In addition to the mophological continuities, genetic analyses of 28S rDNA and COI mitochondrial DNA confirmed that all specimens belong to a single species. Further taxonomic revisions are required to draw conclusions of whether S. markewitschi is a valid species different from S. carpionis, by collecting samples from across their wide distributional ranges, such as Europe, North America, and Northeast Asia. A key to identification of species of Salmincola Wilson, 1915 occurring in Japan is also provided.

Dietary niche breadth influences the effects of urbanization on the gut microbiota of sympatric rodents.

Cities are among the most extreme forms of anthropogenic ecosystem modification, and urbanization processes exert profound effects on animal populations through multiple ecological pathways. Increased access to human-associated food items may alter species' foraging behavior and diet, in turn modifying the normal microbial community of the gastrointestinal tract (GIT), ultimately impacting their health. It is crucial we understand the role of dietary niche breadth and the resulting shift in the gut microbiota as urban animals navigate novel dietary resources. We combined stable isotope analysis of hair and microbiome analysis of four gut regions across the GIT to investigate the effects of urbanization on the diet and gut microbiota of two sympatric species of rodents with different dietary niches: the omnivorous large Japanese field mouse (Apodemus speciosus) and the relatively more herbivorous gray red-backed vole (Myodes rufocanus). Both species exhibited an expanded dietary niche width within the urban areas potentially attributable to novel anthropogenic foods and altered resource availability. We detected a dietary shift in which urban A. speciosus consumed more terrestrial animal protein and M. rufocanus more plant leaves and stems. Such changes in resource use may be associated with an altered gut microbial community structure. There was an increased abundance of the presumably probiotic Lactobacillus in the small intestine of urban A. speciosus and potentially pathogenic Helicobacter in the colon of M. rufocanus. Together, these results suggest that even taxonomically similar species may exhibit divergent responses to urbanization with consequences for the gut microbiota and broader ecological interactions.

Potential negative effects and heterogeneous distribution of a parasitic copepod Salmincola edwardsii (Copepoda: Lernaeopodidae) on Southern Asian Dolly Varden Salvelinus curilus in Hokkaido, Japan.

The genus Salmincola is an ectoparasitic copepod group commonly infesting the branchial and buccal cavities of salmonids. While negative impacts on hatchery fishes have been reported, their impacts on wild fish populations and distribution patterns are critically understudied. In the Shiretoko Peninsula, Hokkaido, Japan, we found parasites belonging to this genus on the branchial cavity of a stream salmonid, Southern Asian Dolly Varden Salvelinus curilus. All parasites recovered were identified as Salmincola edwardsii based on morphological characteristics and partial 28S rDNA sequences. Prevalence was highly heterogeneous even among neighboring streams (0-54.8%, < 10 km) with the mean intensity among streams being generally low (2.19 parasites/infeted fish). Despite the low intensity, quantile regression analysis showed negative trends between parasite intensity and host condition, suggesting that the infestation of S. edwardsii has a potential negative impact on the host salmonid. In addition, a single copepod was found from an anadromous fish, which could indicate some salinity tolerance of the copepods. It is important to evaluate the effects of Salmincola spp. on host species and determine the limiting factors on the parasite's distribution for proper management.

Comparing the gut microbiome along the gastrointestinal tract of three sympatric species of wild rodents.

Host-microbe interactions within the gastrointestinal tract (GIT) play a pivotal role in shaping host physiology, ecology, and life history. However, these interactions vary across gut regions due to changes in the physical environment or host immune system activity, thereby altering the microbial community. Each animal species may harbor their own unique microbial community due to host species-specific ecological traits such as dietary habits, micro-habitat preferences, and mating behavior as well as physiological traits. While the gut microbiota in wild animals has received much attention over the last decade, most studies comparing closely related species only utilized fecal or colon samples. In this study, we first compared the gut microbial community from the small intestine, cecum, colon, and rectum within three sympatric species of wild rodents (i.e. Apodemus speciosus, A. argenteus, and Myodes rufocanus). We then compared each gut region among host species to determine the effect of both gut region and host species on the gut microbiota. We found that the small intestine harbored a unique microbiome as compared to the lower GIT in all three host species, with the genus Lactobacillus in particular having higher abundance in the small intestine of all three host species. There were clear interspecific differences in the microbiome within all gut regions, although some similarity in alpha diversity and community structure within the small intestine was found. Finally, fecal samples may be appropriate for studying the lower GIT in these species, but not the small intestine.

Evidence for Introgressive Hybridization between Native Dolly Varden (Salvelinus curilus (syn. Salvelinus malma)) and Introduced Brook Trout (Salvelinus fontinalis) in the Nishibetsu River of Hokkaido, Japan.

Hybridization is one of the negative outcomes for the introduction of non-native species, which can lead to rapid displacement and genetic extinction of native species. Salmonid fishes have been widely introduced outside of their native ranges for food supply and recreational fishing. Here, we investigate the occurrence of introgressive hybridization among native Dolly Varden (Salvelinus curilus (syn. Salvelinus malma)), white-spotted charr (Salvelinus leucomaenis), and introduced brook trout (Salvelinus fontinalis), in streams of the Nishibetsu River, Hokkaido, Japan. Microsatellite DNA analysis detected five hybrids between native Dolly Varden and introduced brook trout. This is the first evidence for hybridization between native Dolly Varden and introduced brook trout, while the latter has been known to hybridize with many other salmonids. Furthermore, incongruence between mitochondrial DNA and microsatellite DNA analyses suggested introgression among the three Salvelinus species. Further studies to estimate the hybrid fitness are necessary to understand how hybridization among the three species affects the native species.

Characteristics of urban environments and novel problem-solving performance in Eurasian red squirrels.

Urban environments can be deemed 'harsh' for some wildlife species, but individuals frequently show behavioural flexibility to cope with challenges and demands posed by life in the city. For example, urban animals often show better performance in solving novel problems than rural conspecifics, which helps when using novel resources under human-modified environments. However, which characteristics of urban environments fine-tune novel problem-solving performance, and their relative importance, remain unclear. Here, we examined how four urban environmental characteristics (direct human disturbance, indirect human disturbance, size of green coverage and squirrel population size) may potentially influence novel problem-solving performance of a successful 'urban dweller', the Eurasian red squirrel, by presenting them with a novel food-extraction problem. We found that increased direct human disturbance, indirect human disturbance and a higher squirrel population size decreased the proportion of solving success at the population level. At the individual level, an increase in squirrel population size decreased the latency to successfully solve the novel problem the first time. More importantly, increased direct human disturbance, squirrel population size and experience with the novel problem decreased problem-solving time over time. These findings highlight that some urban environmental characteristics shape two phenotypic extremes in the behaviour-flexibility spectrum: individuals either demonstrated enhanced learning or they failed to solve the novel problem.

Temperature-Dependent Swimming Performance Differs by Species: Implications for Condition-Specific Competition between Stream Salmonids.

Condition-specific competition is a phenomenon by which inter-specific competitive dominance changes as a result of environment, and is an important factor determining species distribution. Congeneric charrs in Hokkaido, Japan, provide one of the best examples of condition-specific competition: Dolly Varden, Salvelinus malma, often dominate in cold streams (6-8°C), whereas white-spotted charr, Salvelinus leucomaenis, dominate in warmer streams (> 10°C). While past laboratory and field experiments have demonstrated the great advantage of white-spotted charr at higher water temperatures, the advantages of Dolly Varden at lower temperature have not always been clear. Here, we examined the effect of water temperature (6°C vs. 12°C) on the swimming ability of the two sympatric charrs using a stamina tunnel. At 6°C, the swimming ability of Dolly Varden was greater than that of white-spotted charr, but no difference was observed at 12°C. These results suggest that the temperature-mediated swimming ability differs between these species, which may explain the coexistence of the closely related species within heterogeneous habitats via condition-specific competition.

Comparison of the intestinal helminth community of the large Japanese field mouse (Apodemus speciosus) between urban, rural, and natural sites in Hokkaido, Japan.

Anthropogenic ecosystem modification has affected over 80% of the global land cover. Interest in its effects on wildlife has been growing over the past several decades, specifically in regard to biodiversity and ecosystem function. Parasites are of particular interest, because they directly impact animal health, and can be transmitted to humans through the process of zoonosis. However, most studies so far tended to focus on only one or two parasites with few looking at the entire community, thereby limiting our understanding of the effects of ecosystem modification on parasitic organisms. In this study, we estimated the intestinal helminth diversity and species richness of the large Japanese field mouse (Apodemus speciosus), as well as the prevalence and abundance of each species in two modified ecosystems, a rural agricultural area and an urban park. We then compared them to a natural area to see how they have been altered. We found that diversity, prevalence, and abundance were all highly altered within both modified ecosystems, but generally to a greater degree within the urban park. However, there was great variation in the direction and degree of response of each helminth species, suggesting that generalized trends may be difficult to ascertain. Furthermore, it is important to analyze the entire helminth community, because interspecific interactions and the effect that ecosystem modification has on them may help determine what species persist.

Maladaptive secondary sexual characteristics reduce the reproductive success of hybrids between native and non-native salmonids.

Human-mediated hybridization between introduced and native species is one of the most serious threats to native taxa. Although field studies have attempted to quantify the relative fitness or reproductive success of parental species and their hybrids, only a few studies have unraveled the factors determining the fitness of hybrids. Here, we hypothesized that maladaptive secondary sexual characteristics may reduce fitness of hybrids between two fish species. To test this, we evaluated the reproductive success of introduced brook trout (BT: Salvelinus fontinalis), native white-spotted charr (WSC: S. leucomaenis) and their hybrids in a natural stream in Hokkaido, Japan, where the two parental species show remarkably different male secondary sexual characteristics, such as elongated jaws and deeper bodies. We predicted that introgression from WSC is maladaptive for BT males because the BT male has more prominent secondary sexual characteristics. Our results suggest that both sexual selection and outbreeding depression in males and females significantly influence an individual's reproductive success. Our results also suggest that asymmetric introgression may increase the risks to persistence in the recipient species.

Seasonal and Diel Activity Patterns of Eight Sympatric Mammals in Northern Japan Revealed by an Intensive Camera-Trap Survey.

The activity patterns of mammals are generally categorized as nocturnal, diurnal, crepuscular (active at twilight), and cathemeral (active throughout the day). These patterns are highly variable across regions and seasons even within the same species. However, quantitative data is still lacking, particularly for sympatric species. We monitored the seasonal and diel activity patterns of terrestrial mammals in Hokkaido, Japan. Through an intensive camera-trap survey a total of 13,279 capture events were recorded from eight mammals over 20,344 camera-trap days, i.e., two years. Diel activity patterns were clearly divided into four categories: diurnal (Eurasian red squirrels), nocturnal (raccoon dogs and raccoons), crepuscular (sika deer and mountain hares), and cathemeral (Japanese martens, red foxes, and brown bears). Some crepuscular and cathemeral mammals shifted activity peaks across seasons. Particularly, sika deer changed peaks from twilight during spring-autumn to day-time in winter, possibly because of thermal constraints. Japanese martens were cathemeral during winter-summer, but nocturnal in autumn. We found no clear indication of predator-prey and competitive interactions, suggesting that animal densities are not very high or temporal niche partitioning is absent among the target species. This long-term camera-trap survey was highly cost-effective and provided one of the most detailed seasonal and diel activity patterns in multiple sympatric mammals under natural conditions.

Absolute versus Relative Assessments of Individual Status in Status-Dependent Strategies in Stochastic Environments.

Status-dependent strategies represent one of the most remarkable adaptive phenotypic plasticities. A threshold value for individual status (e.g., body size) is assumed above and below which each individual should adopt alternative tactics to attain higher fitness. This implicitly assumes the existence of an "absolute" best threshold value, so each individual chooses a tactic only on the basis of its own status. However, animals may be able to assess their status on the basis of surrounding individuals. This "relative" assessment considers a threshold value to be changeable depending on individual situations, which may result in significant differences in ecological and evolutionary dynamics compared with absolute assessment. Here, we incorporated Bayesian decision-making and adaptive dynamics frameworks to explore the conditions necessary for each type of assessment to evolve. Our model demonstrates that absolute assessment is always an evolutionarily stable strategy (ESS) in a stable environment, whereas relative assessment can be an ESS in stochastic environments. The consequences of future environmental change differ considerably depending on the assessment chosen. Our results underscore the need to better understand how individuals assess their own status when choosing alternative tactics.

The fishermen were right: experimental evidence for tributary refuge hypothesis during floods.

Fishermen often anecdotally report an unexpected increase of fish caught in small tributary streams during floods, presumably due to refuge-seeking behavior from the main stem. From a population perspective, this implies the significance of refuge habitats and connectivity for population viability against natural disturbances. Despite the plausibility, however, surprisingly few studies have examined the tributary refuge hypothesis, mainly due to the difficulty in field survey during floods. Here, we made use of a large-scale controlled flood to assess whether fishes move into tributaries during flooding in the main stem. A planned water release from the Satsunai River Dam located on Hokkaido Island in Japan rapidly increased the main stem discharge by more than 20-fold. Before, during, and after flooding censuses in four tributaries provided evidence of the refuge-seeking behavior of fishes from the main stem. For example, more than 10 Dolly Varden char, a salmonid fish, were caught in a tributary during the flood, even though almost no individuals were captured before or after the flood. The fish responded immediately to the flooding, suggesting the need for studies during disturbances. In addition, the likelihood of refuge movements varied among tributaries, suggesting the importance of local environmental differences between tributary and the main stem habitats. This is the first study to experimentally confirm the tributary refuge hypothesis, and underscores the roles of habitat diversity and connectivity during disturbances, even though some habitats are not used during normal conditions.

Fine scale relationships between sex, life history, and dispersal of masu salmon.

Identifying the patterns and processes driving dispersal is critical for understanding population structure and dynamics. In many organisms, sex-biased dispersal is related to the type of mating system. Considerably, less is known about the influence of life-history variability on dispersal. Here we investigated patterns of dispersal in masu salmon (Oncorhynchus masou) to evaluate influences of sex and life history on dispersal. As expected, assignment tests and isolation by distance analysis revealed that dispersal of marine-migratory masu salmon was male-biased. However, dispersal of resident and migratory males did not follow our expectation and marine-migratory individuals dispersed more than residents. This may be because direct competition between marine-migratory and resident males is weak or that the cost of dispersal is smaller for marine-migratory individuals. This study revealed that both sex and migratory life-history influence patterns of dispersal at a local scale in masu salmon.

Loss of genetic diversity means loss of geological information: the endangered Japanese crayfish exhibits remarkable historical footprints.

Intra-specific genetic diversity is important not only because it influences population persistence and evolutionary potential, but also because it contains past geological, climatic and environmental information. In this paper, we show unusually clear genetic structure of the endangered Japanese crayfish that, as a sedentary species, provides many insights into lesser-known past environments in northern Japan. Over the native range, most populations consisted of unique 16S mtDNA haplotypes, resulting in significant genetic divergence (overall F(ST) = 0.96). Owing to the simple and clear structure, a new graphic approach unraveled a detailed evolutionary history; regional crayfish populations were comprised of two distinct lineages that had experienced contrasting demographic processes (i.e. rapid expansion vs. slow stepwise range expansion) following differential drainage topologies and past climate events. Nuclear DNA sequences also showed deep separation between the lineages. Current ocean barriers to dispersal did not significantly affect the genetic structure of the freshwater crayfish, indicating the formation of relatively recent land bridges. This study provides one of the best examples of how phylogeographic analysis can unravel a detailed evolutionary history of a species and how this history contributes to the understanding of the past environment in the region. Ongoing local extinctions of the crayfish lead not only to loss of biodiversity but also to the loss of a significant information regarding past geological and climatic events.

A case of isolation by distance and short-term temporal stability of population structure in brown trout (Salmo trutta) within the River Dart, southwest England.

Salmonid fishes exhibit high levels of population differentiation. In particular, the brown trout (Salmo trutta L.) demonstrates complex within river drainage genetic structure. Increasingly, these patterns can be related to the underlying evolutionary models, of which three scenarios (member-vagrant hypothesis, metapopulation model and panmixia) facilitate testable predictions for investigations into population structure. We analysed 1225 trout collected from the River Dart, a 75 km long river located in southwest England. Specimens were collected from 22 sample sites across three consecutive summers (2001-2003) and genetic variation was examined at nine microsatellite loci. A hierarchical analysis of molecular variance revealed that negligible genetic variation was attributed among temporal samples. The highest levels of differentiation occurred among samples isolated above barriers to fish movement, and once these samples were removed, a significant effect of isolation-by-distance was observed. These results suggest that, at least in the short-term, ecological events are more important in shaping the population structure of Dart trout than stochastic extinction events, and certainly do not contradict the expectations of a member-vagrant hypothesis. Furthermore, individual-level spatial autocorrelation analyses support previous recommendations for the preservation of a number of spawning sites spaced throughout the tributary system to conserve the high levels of genetic variation identified in salmonid species.

Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr.

Isolation by distance is usually tested by the correlation of genetic and geographic distances separating all pairwise populations' combinations. However, this method can be significantly biased by only a few highly diverged populations and lose the information of individual population. To detect outlier populations and investigate the relative strengths of gene flow and genetic drift for each population, we propose a decomposed pairwise regression analysis. This analysis was applied to the well-described one-dimensional stepping-stone system of stream-dwelling Dolly Varden charr (Salvelinus malma). When genetic and geographic distances were plotted for all pairs of 17 tributary populations, the correlation was significant but weak (r(2) = 0.184). Seven outlier populations were determined based on the systematic bias of the regression residuals, followed by Akaike's information criteria. The best model, 10 populations included, showed a strong pattern of isolation by distance (r(2) = 0.758), suggesting equilibrium between gene flow and genetic drift in these populations. Each outlier population was also analysed by plotting pairwise genetic and geographic distances against the 10 nonoutlier populations, and categorized into one of the three patterns: strong genetic drift, genetic drift with a limited gene flow and a high level of gene flow. These classifications were generally consistent with a priori predictions for each population (physical barrier, population size, anthropogenic impacts). Combined the genetic analysis with field observations, Dolly Varden in this river appeared to form a mainland-island or source-sink metapopulation structure. The generality of the method will merit many types of spatial genetic analyses.