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Osamu Kishida
Field Science Center for Northern Biosphere　Forest Research Station　Wakayama Experimental Forest
Associate Professor
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Last Updated :2024/05/09

Researcher Profile and Settings

Affiliation

  • Field Science Center for Northern Biosphere　Forest Research Station　Wakayama Experimental Forest

Job Title

  • Associate Professor

Degree

  • Ph. D（Hokkaido University）

URL

J-Global ID

Research Interests

  • アズマヒキガエル   外来種   誘導防御   表現型可塑性   誘導攻撃   間接効果   生態系機能   形態変化   エゾサンショウウオ   適応   捕食   相互作用   エゾアカガエル   両生類   栄養カスケード   メソコスム   遺伝学   動物   生態学   個体群生態学   群集生態学   行動生態学   進化生態学   Community Ecology   Evolutionary Ecology   

Research Areas

  • Life sciences / Ecology and environmental science

Educational Organization

Academic & Professional Experience

  • 2012/11 - Today Hokkaido University Field Science Center for Northern Biosphere
  • 2009/04 - 2012/10 Hokkaido University Field Science Center for Northern Biosphere

Research Activities

Published Papers

  • Hiroto Endo, Hiromi Uno, Osamu Kishida, Kentaro Morita
    Japanese Journal of Conservation Ecology 28 (2) 453 - 465 2023/12 [Refereed]
  • Weili Shi, Zhongliang Zhou, Benjamin H. Letcher, Nathaniel Hitt, Yoichiro Kanno, Ryo Futamura, Osamu Kishida, Kentaro Morita, Sheng Li
    Lecture Notes in Computer Science 252 - 264 0302-9743 2023/11/27
  • Hisanori Okamiya, Osamu Kishida
    Population Ecology 1438-3896 2022/02/08
  • Ryo Futamura, Kentaro Morita, Yoichiro Kanno, Shoji Kumikawa, Yuichi Matsuoka, Atsushi Okuda, Hiroshi Sugiyama, Hiroyuki Takahashi, Jiro Uchida, Osamu Kishida
    Oecologia 0029-8549 2022/01/22 [Refereed]
     
    In many migratory species, smaller migrants suffer higher mortality rates during the risky migration. To minimize the size-selective mortality, migrants with smaller body sizes would need to accelerate growth rates or delay migration timing to attain a large enough body size prior to migration. To test these predictions, we investigated size-dependent patterns of growth rates and migration timing of juvenile masu salmon (Oncorhynchus masou) before their oceanic migration. We tracked uniquely marked individuals in a study population consisted of oceanic migrants and river-dwelling residents using mark-recapture surveys and PIT-tag antenna-reader system. Data supported our predictions about size-dependent growth rates and migration timing. For approximately 6 months before outmigration (i.e., between the decision of migration and the start of migration), eventual migrants grew more than residents if their initial size was smaller, but such a difference in growth rate diminished for fish with larger initial sizes. In addition, smaller eventual migrants delayed the timing of outmigration compared to larger individuals, to attain a larger body size in the river prior to migration. These results suggest that size-selective mortality during migration has shaped size-dependent patterns of the pre-migration growth in migratory masu salmon. Size-conditional changes in growth rate and duration of pre-migration period may be an adaptive tactic for the migratory animals.
  • Ryo Futamura, Kentaro Morita, Yoichiro Kanno, Osamu Kishida
    Environmental Biology of Fishes 105 (12) 1833 - 1843 0378-1909 2022/01/17 [Refereed]
  • Samuel R. P.‐J. Ross, Jorge García Molinos, Atsushi Okuda, Jackson Johnstone, Keisuke Atsumi, Ryo Futamura, Maureen A. Williams, Yuichi Matsuoka, Jiro Uchida, Shoji Kumikawa, Hiroshi Sugiyama, Osamu Kishida, Ian Donohue
    Global Change Biology 28 (2) 403 - 416 1354-1013 2022/01 [Refereed]
     
    Amidst the global extinction crisis, climate change will expose ecosystems to more frequent and intense extreme climatic events, such as heatwaves. Yet, whether predator species loss-a prevailing characteristic of the extinction crisis-will exacerbate the ecological consequences of extreme climatic events remains largely unknown. Here, we show that the loss of predator species can interact with heatwaves to moderate the compositional stability of ecosystems. We exposed multitrophic stream communities, with and without a dominant predator species, to realistic current and future heatwaves and found that heatwaves destabilised algal communities by homogenising them in space. However, this happened only when the predator was absent. Additional heatwave impacts on multiple aspects of stream communities, including changes to the structure of algal and macroinvertebrate communities, as well as total algal biomass and its temporal variability, were not apparent during heatwaves and emerged only after the heatwaves had passed. Taken together, our results suggest that the ecological consequences of heatwaves can amplify over time as their impacts propagate through biological interaction networks, but the presence of predators can help to buffer such impacts. These findings underscore the importance of conserving trophic structure, and highlight the potential for species extinctions to amplify the effects of climate change and extreme events.
  • Ryo Futamura, Kentaro Morita, Koume Araki, Masato Ayumi, Shoji Kumikawa, Yuichi Matsuoka, Atsushi Okuda, Hiroshi Sugiyama, Hiroyuki Takahashi, Taro Takahashi, Jiro Uchida, Osamu Kishida
    Ichthyological Research 69 (1) 194 - 196 1341-8998 2022/01
  • Hiroki Mizumoto, Osamu Kishida, Kotaro Takai, Naru Matsuura, Hitoshi Araki
    Biological Invasions 24 (4) 1199 - 1211 1387-3547 2021/12/15 [Refereed]
     
    AbstractUnderstanding the distribution of invasive species and their reproductive area is crucial for their managements after invasion. While catch and observation surveys are still embraced, environmental DNA (eDNA) has been increasingly utilized as an efficient tool for identifying these species in the wild. In this study, we developed a Bufo-specific eDNA assay for detecting an invasive, toxic, and terrestrial toad species Bufo japonicus formosus in Hokkaido, Japan, and applied it to their reproductive area at watershed scale. The eDNA assay was field-validated in ponds where B. japonicus were observed, as well as in rivers downstream of the reproductive ponds. Thus, the assay provided us an opportunity to screen watersheds that include their reproductive area by collecting downstream water samples. Applying it to the Ishikari river basin, the largest river basin in Hokkaido (c.a., 14,330 km2), we detected toad eDNA at 32 out of 73 sampling sites. They are composed of eleven sites with species observation records nearby (all the sites with observation records within a 500 m radius) and 21 sites without such records. And those eDNA detections were from twelve out of 31 river systems in the entire river basin. A Bayesian, multiscale occupancy model supported high eDNA detectability among those sites. These results suggest that the eDNA assay can efficiently estimate the presence of reproductive area of the terrestrial toad even from a distant downstream of the watershed, and that it provides a powerful means of detecting new reproductive area and monitoring further spread of invasive species.
  • Hiromi Uno, Mizushi Yokoi, Keitaro Fukushima, Yoichiro Kanno, Osamu Kishida, Wataru Mamiya, Rei Sakai, Shunsuke Utsumi
    Freshwater Biology 67 (3) 549 - 563 0046-5070 2021/12/09 [Refereed]
     
    Diverse aquatic environments in floodplains support high biodiversity, including plankton, benthos, nekton (fish), and amphibians. Variation in aquatic communities among waterbodies should be explained not only by the spatial variation in the environment at low flow but also by the hydrological dynamics and biological responses over flood and recession periods. However, very few studies have examined the formation processes of floodplain aquatic communities over flood periods. In this study, we aimed to obtain a mechanistic understanding of the assembly of aquatic communities on a temperate floodplain by conducting intensive fieldwork during and after seasonal flooding. The study was conducted in the Butokamabetsu River catchment in northern Hokkaido, where snowmelt causes annual spring floods. At peak flow, floodwater not only flow through main stream river and the extant side channels, but also flow through some palaeo-side channels, which are usually isolated from the mainstream river and harbour stagnant water. As the floods recede, palaeo-side channels become isolated from the mainstream river and their flow cease, but the timing of the flow cessation varied among palaeo-side channels. We hypothesised that this spatial asynchrony in the timing of flow cessations shapes diverse floodplain aquatic communities. Therefore, we conducted field surveys of four faunal groups (plankton, benthos, nekton [fish], and amphibian) during and after the spring flood in 2019. The post-flood aquatic communities varied spatially, according to the flow at peak flood, the timing of flow cessation, and the flow at low flow. Plankton composition was influenced by the water flow at peak flood, and they were more abundant in waterbodies that were never flushed by floodwaters. Fish composition was also influenced by the water flow at peak flood; in particular, salmonids were more abundant in waterbodies that were hydrologically connected to the main stream at peak flood. The presence of amphibian eggs was influenced by the timing of flow cessation; eggs were laid in waterbodies with stagnant water during breeding season. The benthic composition was influenced by flow at low flow. After the flood had receded, these different distribution patterns of the four biological groups led to gradual variation of aquatic communities among waterbodies on a floodplain. Overall, this study showed that hydrological dynamics during flood recession shapes the post-flood aquatic communities, and the spatial variability in the hydrological dynamics and the different responses of the four faunal groups support diverse aquatic communities on a floodplain. Importance of the natural geomorphological complexities, where paleo-side channels with wide range of hydrological connectivity to the river channel co-occur, as well as the natural hydrological dynamics of snowmelt recession, where the flooding discharge gradually decrease over a certain period in spring for floodplain aquatic communities are highlighted.
  • Hisanori Okamiya, Ryohei Sugime, Chiharu Furusawa, Yoshihiro Inoue, Osamu Kishida
    Zoological Letters 7 (14) 2021/12 [Refereed]
     
    AbstractAlthough paedomorphosis is widespread across salamander families, only two species have ever been documented to exhibit paedomorphosis in Hynobiidae. One of these two exceptional species is Hynobius retardatus in which paedomorphosis was first reported in 1924, in specimens from Lake Kuttara in Hokkaido. This population became extinct after the last observation in 1932; since then, no paedomorphs of this species have been reported anywhere. Here, we report the rediscovery of paedomorphs of this species. Three paedomorph-like male salamanders were collected from a pond in the south Hokkaido in December 2020 and April 2021; in size, these specimens were similar to metamorphosed adults but they still displayed larval features such as external gills and a well-developed caudal fin. An artificial fertilization experiment demonstrated that they were sexually compatible with metamorphosed females, thus, confirming them to be paedomorphs. Future efforts to find additional paedomorphs in this and other populations are required to assess the prevalence of paedomorphosis in H. retardatus and to improve understanding of the ecology and evolution of paedomorphisis in Urodela.
  • Hisanori Okamiya, Masataka Tagami, Michael Crossland, Osamu Kishida
    Hydrobiologia 848 (19) 4445 - 4452 0018-8158 2021/11 [Refereed]
  • Yoichiro Kanno, Audrey C. Harris, Osamu Kishida, Shunsuke Utsumi, Hiromi Uno
    Ecology of Freshwater Fish 0906-6691 2021/09/04 [Refereed]
     
    Movement patterns of stream fish vary individually, but little is known about how a set of individual characteristics affect movement at multiple spatial scales. We investigated the effect of body length and condition (i.e. weight relative to length) on emigration from a tributary and movement within the tributary during summer in Japanese salmonids (white-spotted charr Salvelinus leucomaenis and masu salmon Oncorhynchus masou) using mark-recapture and PIT antenna technology. Emigration from the tributary was influenced more strongly by body length than by body condition, whereas movement within the tributary (> 20 m) was influenced by body condition and their interaction with body length. Specifically, larger individuals in better body condition were more likely to stay locally (<= 20 m), but smaller individuals in better condition were more likely to move in the tributary. We discuss benefits and costs of movement that vary with individual characteristics (i.e. body length and condition) and spatial scales. In one instance (charr between June and July), survival rates were lower in smaller individuals, which also were more likely to emigrate from the tributary, suggesting that emigration might have been facilitated by the mortality cost of staying in the tributary. This study indicates that stream fish movement is shaped by complex mechanisms that differ by spatial scale. Although complex, two study species often responded similarly, indicative of emerging regularities across species in determinants of multi-scale stream fish movement.
  • Hisanori Okamiya, Yoshihiro Inoue, Kotaro Takai, Michael R. Crossland, Osamu Kishida
    Ecological Research 0912-3814 2021/08/30 [Refereed]
  • Kevin A. Fitzgerald, Matt R. Haworth, Kevin R. Bestgen, Collin J. Farrell, Shunsuke Utsumi, Osamu Kishida, Hiromi Uno, Yoichiro Kanno
    Fisheries Management and Ecology 28 (6) 507 - 515 0969-997X 2021/06/29 [Refereed]
     
    Hatch timing in autumn-spawning stream salmonids is poorly understood in the subarctic region because snow cover prevents direct sampling of cryptic early life stages. Otolith micro-increment analysis was used to infer hatch dates of white-spotted charr Salvelinus leucomaenis (Pallas) and masu salmon Oncorhynchus masou (Brevoort) in a mainstem-tributary network in northern Japan. Accuracy and precision were validated by ageing hatchery individuals with known hatch date ranges. In July 2018, 93 wild young-of-the-year white-spotted charr and 81 masu salmon were collected and aged. Masu salmon hatched, on average, 24 days earlier (mean = February 8) than white-spotted charr (March 4), and hatch dates spanned a minimum of 2 months for each species. In masu salmon, hatch dates of individuals collected in the mainstem were nearly 3 weeks earlier than those in a tributary. This study provided knowledge on intra- and inter-specific variation in hatch timing of native salmonids in a subarctic stream network.
  • Hisanori Okamiya, Kotaro Takai, Osamu Kishida
    Current Herpetology 40 (1) 1345-5834 2021/03/02 [Refereed]
  • Noboru Katayama, Osamu Kishida, Chikako Miyoshi, Shintaro Hayakashi, Kinya Ito, Rei Sakai, Aiko Naniwa, Hiroyuki Takahashi, Kentaro Takagi
    PLOS ONE 15 (12) e0243089 - e0243089 2020/12/01 [Refereed]
     
    Anthropogenic disturbances in forest management practices can affect wild edible plants. Soil scarification is a large-scale disturbance that may cause long-term reduction in productivity of edible dwarf bamboo, Sasa kurilensis, in northern Japan. For their effective and sustainable use, we need to understand the recovery process after such disturbances. At 14 study sites in the Teshio Experimental Forest of Hokkaido University where soil scarification had been conducted between 2 and 44 years prior, the number and stem diameter of old and young (newly emerged, edible) culms was recorded. At sites that were within 11 years of soil scarification, the proportion of old culms (<11%) was lower than in the control area where soil scarification had never been conducted. At sites where more than 15 years had passed since soil scarification, the relative number of old culms was nearly equal to that in control area. Additionally, the number of young culms increased with an increasing number of old culms. These results suggest that recovery of productivity (in term of number) of edible culms may take a few decades. In contrast, the culm diameter of young culms increased linearly with time since soil scarification, but the 95% confidence interval in this relationship suggests that dwarf bamboo can produce thick edible culms soon after soil scarification. These findings will provide useful insights into how to obtain high quality bamboo culms following anthropogenic disturbances in future.
  • Masatoshi Matsunami, Toru Miura, Osamu Kishida, Hirofumi Michimae, Kinya Nishimura
    Zoological Science 37 (6) 0289-0003 2020/10/12 [Refereed]
  • Kunio Takatsu, Osamu Kishida
    Journal of Animal Ecology 89 (7) 1615 - 1627 0021-8790 2020/07 [Refereed]
  • Yoichiro Kanno, Naoki Yui, Wataru Mamiya, Rei Sakai, Yuri Yabuhara, Tohru Miyazaki, Shunsuke Utsumi, Osamu Kishida, Hiromi Uno
    Canadian Journal of Fisheries and Aquatic Sciences 77 (6) 1090 - 1100 0706-652X 2020/06 [Refereed]
     
    We studied movement of a native salmonid, white-spotted char (Salvelinus leucomaenis), in a 1-km tributary in northern Hokkaido, Japan, in May–July 2018. Based on physical mark–recapture of 501 unique individuals and detection by mobile PIT antenna over monthly intervals, a majority of fish (70%–80%) stayed within 60 m of previously released locations, demonstrating what appeared to be restricted movement patterns. However, fixed PIT antenna data showed that as much as 17% of marked individuals emigrated from the study area during the 2-month study period. Probability of emigration did not depend on where in the 1-km segment individuals had been released, indicating that emigration likely represented long-distance movement. Once emigrants made a decision to emigrate, they left the tributary within 1–3 median days by moving downstream in a unidirectional manner, based on detections at a total of three antenna arrays deployed throughout the tributary. Our multiscale analysis provided strong support for co-existence of short- and long-distance movement patterns, and we conclude that movement data at multiple spatial scales complement each other to characterize population-scale movement.
  • Keisuke Atsumi, Osamu Kishida
    Ecological Research 35 (3) 533 - 539 0912-3814 2020/05 [Refereed]
  • Nanoko Meguro, Osamu Kishida, Shunsuke Utsumi, Shigeru Niwa, Susumu Igarashi, Chikara Kozuka, Aiko Naniwa, Takuya Sato
    Ecological Research 35 (3) 482 - 493 0912-3814 2020/05 [Refereed][Not invited]
  • Narumi Oyake, Nayuta Sasaki, Aya Yamaguchi, Hiroyuki Fujita, Masataka Tagami, Koki Ikeya, Masaki Takagi, Makoto Kobayashi, Harue Abe, Osamu Kishida
    FRESHWATER BIOLOGY 65 (2) 240 - 252 0046-5070 2020/02 [Refereed][Not invited]
     
    To manage biological invasions effectively, the impacts of alien species on the demography and traits of native species must be known, but determining those impacts can be challenging. We used a comparative approach to gain insight into the impacts that an alien toad (Bufo japonicus formosus) might have on native Japanese predatory amphibians. We compared the susceptibility of native predator species to alien toad toxins in the alien-invaded range and the susceptibility of closely related native predator species to the toxins in the alien toad's native range to investigate the impacts of an alien on a native species. Bufo japonicus formosus is native to Honshu, but was recently introduced to Hokkaido and Sado. In laboratory experiments, we compared individual mortality of predators exposed to a toad hatchling between novel predators on the toad-invaded islands and ecologically similar congeneric or conspecific species on Honshu, where the toad is native. We also compared (1) the percentage of individuals that consumed a toad hatchling and (2) toxin resistance (i.e. survival and growth of individuals after toad consumption) between these two groups of predators, as mechanistic components behind the susceptibility of the predators to the toxic prey. The mortality of Rana pirica from all populations after consumption of a toad hatchling was almost 100%, and that of Hynobius retardatus ranged from 14 to 90%, depending on the population. In contrast, the mortality of Rana ornativentris and Hynobius nigrescens was near 0% regardless of population. These differences between congeneric predators were mostly due to differences in their toxin resistance. These results suggest that the alien toad is a potential threat to the novel amphibian predators on Hokkaido, although they also imply that the novel predators on Hokkaido have the potential to develop toxin resistance through adaptive evolution. However, this counteradaptation may have a higher chance of evolving in H. retardatus than in R. pirica because of differences in their genetic backgrounds.
  • Atsumi Keisuke, Kishida Osamu, Koizum Itsuro
    JOURNAL OF ETHOLOGY 37 (3) 353 - 362 0289-0771 2019/09 [Refereed][Not invited]
  • Terada, Chisato, Kwon, TaeOh, Kazahari, Nobuko, Kishida, Osamu, Utsumi, Shunsuke
    ECOLOGICAL RESEARCH 34 (3) 349 - 349 0912-3814 2019/05 [Refereed][Not invited]
     
    The Forest Research Station of Hokkaido University owns a vast area of experimental forests, which are composed of a large variety of ecosystems ranging from aquatic ecosystems, such as wetlands and river basins, to various types of forests, such as primary, secondary and artificial forests. Additionally, these forests are representative of numerous climatic zones, such as warm temperate, cool temperate and subarctic. Since the initial establishment of the Forest Research Station in 1901, huge efforts have been devoted to recording the vegetation structure and vertebrate assemblages of these experimental forests. Thus, a large body of literature and long-term data on fauna and flora of these forests has been accumulated in our archives. However, most of these records have been written in Japanese and are not opened to the public or well structured. Therefore, we comprehensively reviewed these records and related scientific articles from the 1910s to the 2010s to build up the database for vascular plant and vertebrate animals that inhabited (in the past) and/or are currently inhabiting in the experimental forests. Additional site-specific information was also listed, including geological and topographical characteristics where species were found as well as the localities, survey area and year in which species were recorded. These databases, which span a large temporal and spatial scale, are expected to provide useful data for research or educational purposes and for understanding the flora and fauna of Japan. These can also contribute to a greater understanding of the historical transition of biodiversity in Japan.
  • Kazila Evangelia, Osamu Kishida
    FRESHWATER BIOLOGY 64 (1) 56 - 70 0046-5070 2019/01 [Refereed][Not invited]
  • Masayuki Ushio, Hisato Fukuda, Toshiki Inoue, Kobayashi Makoto, Osamu Kishida, Keiichi Sato, Koichi Murata, Masato Nikaido, Tetsuya Sado, Yukuto Sato, Masamichi Takeshita, Wataru Iwasaki, Hiroki Yamanaka, Michio Kondoh, Masaki Miya
    MOLECULAR ECOLOGY RESOURCES 17 (6) e63 - e75 1755-098X 2017/11 [Refereed][Not invited]
     
    Terrestrial animals must have frequent contact with water to survive, implying that environmental DNA (eDNA) originating from those animals should be detectable from places containing water in terrestrial ecosystems. Aiming to detect the presence of terrestrial mammals using forest water samples, we applied a set of universal PCR primers (MiMammal, a modified version of fish universal primers) for metabarcoding mammalian eDNA. The versatility of MiMammal primers was tested in silico and by amplifying DNAs extracted from tissues. The results suggested that MiMammal primers are capable of amplifying and distinguishing a diverse group of mammalian species. In addition, analyses of water samples from zoo cages of mammals with known species composition suggested that MiMammal primers could successfully detect mammalian species from water samples in the field. Then, we performed an experiment to detect mammals from natural ecosystems by collecting five 500-ml water samples from ponds in two cool-temperate forests in Hokkaido, northern Japan. MiMammal amplicon libraries were constructed using eDNA extracted from water samples, and sequences generated by Illumina MiSeq were subjected to data processing and taxonomic assignment. We thereby detected multiple species of mammals common to the sampling areas, including deer (Cervus nippon), mouse (Mus musculus), vole (Myodes rufocanus), raccoon (Procyon lotor), rat (Rattus norvegicus) and shrew (Sorex unguiculatus). Many previous applications of the eDNA metabarcoding approach have been limited to aquatic/semiaquatic systems, but the results presented here show that the approach is also promising even for forest mammal biodiversity surveys.
  • Kunio Takatsu, Volker H. W. Rudolf, Osamu Kishida
    BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY 120 (3) 675 - 684 0024-4066 2017/03 [Refereed][Not invited]
     
    Predation can strongly influence the evolution of prey species by selecting for defensive phenotypes that reduce the risk of predation. Although cannibalism is frequent in predators and is known to strongly influence predator-prey dynamics, it is largely neglected when studying the evolution of phenotypic defences in prey. Changes in cannibalism can alter the abundance, size-structure, and even phenotypes within predator populations, and thereby change the numerical and per-capita effects driving the selection pressure on defensive phenotypes in prey. In the present study, we experimentally manipulated the presence and absence of cannibalism in predatory salamander larvae Hynobius retardatus (Dunn) and examined how this affects the expression of and selection pressure on inducible defensive phenotype (bulgy phenotype) in its prey, Rana pirica (Matsui) tadpoles. In the absence of cannibalism, salamanders were generally not sufficiently large to consume tadpoles, tadpoles did not express the defensive phenotype, and all phenotypes had equally high survival. By contrast, cannibalism of salamanders accelerated growth rates, leading to the development of 'giant' cannibalistic morphs that were able to consume tadpoles. Importantly, only in the presence of these giant cannibals did tadpoles express a defensive 'bulgy' phenotype that had significantly higher survival rates than phenotypes without this defence, indicating that cannibalism altered the selective regime for defensive traits in prey. The results of the present study demonstrate that cannibalism can drive trait evolution in predator-prey systems and suggest that we cannot predict how changes in numerical effects in predator populations affect selection regimes on prey traits without accounting for concurrent changes in predator per-capita effects. (C) 2016 The Linnean Society of London.
  • Mitsuru Hattori, Osamu Kishida, Takao Itino
    INSECTES SOCIAUX 64 (1) 39 - 44 0020-1812 2017/02 [Refereed][Not invited]
     
    In social insects, intracaste variation suggests the existence of adaptive mechanisms such as polymorphism and polyphenism (i.e., subcastes) for maintaining the sophisticated social system. Here, we investigated intracaste variation patterns of a behavior (i.e., aggressiveness) and of morphology in the soldier caste of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae). This species produces sterile individuals (soldiers), which have larger horns and forelegs than non-soldier reproductive individuals and which specialize in colony defense against predators. We previously showed that in midsummer, when predators are abundant, mother aphids produce soldiers with larger horns and forelegs than they do in early summer, when predators are few. However, the aggressiveness of C. japonica soldiers, another functional trait for colony defense, has not yet been quantified, and the relationship between the expression of this behavioral trait with that of the morphological traits has not yet been examined. Here, we experimentally showed that in midsummer soldiers behave more aggressively in response to artificial stimuli mimicking contact with a predator than they do in early summer. Furthermore, this variation correlated with the phenological variation of defensive morphology in soldier aphids. These results suggest that C. japonica defend their colony with not only strengthening soldier's morphological weapon but also strengthening soldier's aggressiveness when predator risk is high.
  • Aya Yamaguchi, Kunio Takatsu, Osamu Kishida
    ECOLOGY 97 (11) 3206 - 3218 0012-9658 2016/11 [Refereed][Not invited]
     
    Size variation within a population can influence the structure of ecosystem interactions, because ecological performance differs between individuals of different sizes. Although the impact of size variation in a predator species on the structure of interactions is well understood, our knowledge about how size variation in a prey species might modify the interactions between predators and prey is very limited. Here, by examining the interactions between predatory Hynobius retardatus salamander larvae and their prey, Rana pirica frog tadpoles, we investigated how large prey individuals affect the predation mortality of small prey conspecifics. First, in an experiment conducted in a field pond in which we manipulated the presence of salamanders and large tadpoles (i.e., large enough to protect them against salamander predation) with small tadpoles, we showed that in the presence of large tadpoles the mortality of small tadpoles from salamander predation was increased. On the basis of our observations of the activity of individuals, we hypothesized that active large tadpoles caused physical disturbances, which in turn caused the small tadpoles to move, and thus increased their encounter frequency with the predatory salamanders. To test this hypothesis, we conducted a laboratory experiment in small tanks with three players (i.e., one salamander as predator, one small tadpole as focal prey, and either a small or a large tadpole as the prospective movement inducer). In each tank, we manipulated the presence or absence of a movement inducer, and, when present, its size (large or small) and access (caged or uncaged) to the focal prey. In the presence of a large, uncaged movement inducer, the focal prey was more active and suffered from higher predation mortality compared with the other treatments, because the large movement inducer (unlike a small movement inducer) moved actively and, when uncaged, could stimulate movement of the focal prey through direct contact. The results indicated that high activity of large prey individuals and the resulting behavioral interactions with small conspecifics via direct contact indirectly increased the mortality of the small prey.
  • Hirokazu Toju, Osamu Kishida, Noboru Katayama, Kentaro Takagi
    PLOS ONE 11 (11) 1932-6203 2016/11 [Refereed][Not invited]
     
    Fungi in soil play pivotal roles in nutrient cycling, pest controls, and plant community succession in terrestrial ecosystems. Despite the ecosystem functions provided by soil fungi, our knowledge of the assembly processes of belowground fungi has been limited. In particular, we still have limited knowledge of how diverse functional groups of fungi interact with each other in facilitative and competitive ways in soil. Based on the high-throughput sequencing data of fungi in a cool-temperate forest in northern Japan, we analyzed how taxonomically and functionally diverse fungi showed correlated fine-scale distributions in soil. By uncovering pairs of fungi that frequently co-occurred in the same soil samples, networks depicting fine-scale co-occurrences of fungi were inferred at the O (organic matter) and A (surface soil) horizons. The results then led to the working hypothesis that mycorrhizal, endophytic, saprotrophic, and pathogenic fungi could form compartmentalized (modular) networks of facilitative, antagonistic, and/or competitive interactions in belowground ecosystems. Overall, this study provides a research basis for further understanding how interspecific interactions, along with sharing of niches among fungi, drive the dynamics of poorly explored biospheres in soil.
  • Noboru Katayama, Kobayashi Makoto, Osamu Kishida
    PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 283 (1839) 20160996  0962-8452 2016/09 [Refereed][Not invited]
     
    Conventional food-web theory assumes that nutrients from dissolved organic matter are transferred to aquatic vertebrates via long nutrient pathways involving multiple eukaryotic species as intermediary nutrient transporters. Here, using larvae of the salamander Hynobius retardatus as a model system, we provide experimental evidence of a shortcut nutrient pathway by showing that H. retardatus larvae can use dissolved amino acids for their growth without eukaryotic mediation. First, to explore which amino acids can promote larval growth, we kept individual salamander larvae in one of eight different high-concentration amino acid solutions, or in control water from which all other eukaryotic organisms had been removed. We thus identified five amino acids (lysine, threonine, serine, phenylalanine, and tyrosine) as having the potential to promote larval growth. Next, using N-15-labelled amino acid solutions, we demonstrated that nitrogen from dissolved amino acids was found in larval tissues. These results suggest that salamander larvae can take up dissolved amino acids from environmental water to use as an energy source or a growth-promoting factor. Thus, aquatic vertebrates as well as aquatic invertebrates may be able to use dissolved organic matter as a nutrient source.
  • Aya Yamaguchi, Osamu Kishida
    SALAMANDRA 52 (1) 45 - 47 0036-3375 2016/04 [Refereed][Not invited]
  • Aya Yamaguchi, Osamu Kishida
    OIKOS 125 (2) 271 - 277 0030-1299 2016/02 [Refereed][Not invited]
     
    Intrapopulation size variation strongly influences ecological interactions because individuals belonging to different size groups have distinct functions. Most demonstrations of the impacts of size variation in trophic systems have focused on size variation in predator species, and the consequences of size variation in prey species are less well understood. We investigated how prey size structure shapes intra- and interspecific interactions in experiments with a gape-limited predator (larvae of the salamander Hynobius retardatus) and its heterospecific prey (frog tadpoles, Rana pirica). We found that large and small tadpole size groups each increased mortality in the other group by intensifying salamander predation; this type of indirect interactions is called apparent competition. The antagonistic impacts on the prey size groups were caused by different size-specific mechanisms. By consuming small tadpoles, the salamanders grew large enough to consume large tadpoles. The activity of large tadpoles, by increasing the activity of the small tadpoles, may increase the number of encounters with the predator and thus small tadpole mortality. These results suggest that the magnitude of a predator's ecological role, such as whether a top-down trophic cascade is initiated, depends on size variation in its heterospecific prey.
  • Noboru Katayama, Osamu Kishida, Rei Sakai, Shintaro Hayakashi, Chikako Miyoshi, Kinya Ito, Aiko Naniwa, Aya Yamaguchi, Katsunori Wada, Shiro Kowata, Yoshinobu Koike, Katsuhiro Tsubakimoto, Kenichi Ohiwa, Hirokazu Sato, Toru Miyazaki, Shinichi Oiwa, Tsubasa Oka, Shinya Kikuchi, Chikako Igarashi, Shiho Chiba, Yoko Akiyama, Hiroyuki Takahashi, Kentaro Takagi
    PLOS ONE 10 (12) e0146228 - e0146228 1932-6203 2015/12/31 [Refereed]
     
    Wild edible plants, ecological foodstuffs obtained from forest ecosystems, grow in natural fields, and their productivity depends on their response to harvesting by humans. Addressing exactly how wild edible plants respond to harvesting is critical because this knowledge will provide insights into how to obtain effective and sustainable ecosystem services from these plants. We focused on bamboo shoots of Sasa kurilensis, a popular wild edible plant in Japan. We examined the effects of harvesting on bamboo shoot productivity by conducting an experimental manipulation of bamboo shoot harvesting. Twenty experimental plots were prepared in the Teshio Experimental Forest of Hokkaido University and were assigned into two groups: a harvest treatment, in which newly emerged edible bamboo shoots were harvested (n = 10); and a control treatment, in which bamboo shoots were maintained without harvesting (n = 10). In the first year of harvesting (2013), bamboo shoot productivities were examined twice; i.e., the productivity one day after harvesting and the subsequent post-harvest productivity (2-46 days after harvesting), and we observed no difference in productivity between treatments. This means that there was no difference in original bamboo shoot productivity between treatments, and that harvesting did not influence productivity in the initial year. In contrast, in the following year (2014), the number of bamboo shoots in the harvested plots was 2.4-fold greater than in the control plots. These results indicate that over-compensatory growth occurred in the harvested plots in the year following harvesting. Whereas previous research has emphasized the negative impact of harvesting, this study provides the first experimental evidence that harvesting can enhance the productivity of a wild edible plant. This suggests that exploiting compensatory growth, which really amounts to less of a decline in productivity, may be s a key for the effective use of wild edible plants.
  • Zacharia J. Costa, Osamu Kishida
    OECOLOGIA 178 (4) 1215 - 1225 0029-8549 2015/08 [Refereed][Not invited]
     
    Predicting the impacts of climate change on communities requires understanding how temperature affects predator-prey interactions under different biotic conditions. In cases of size-specific predation, environmental influences on the growth rate of one or both species can determine predation rates. For example, warming increases top-down control of food webs, although this depends on resource availability for prey, as increased resources may allow prey to reach a size refuge. Moreover, because the magnitude of inducible defenses depends on predation rates and resource availability for prey, temperature and resource levels also affect phenotypic plasticity. To examine these issues, we manipulated the presence/absence of predatory Hynobius retardatus salamander larvae and herbivorous Rana pirica tadpoles at two temperatures and three basal resource levels. and measured their morphology, behavior, growth and survival. Prior work has shown that both species express antagonistic plasticity against one another in which salamanders enlarge their gape width and tadpoles increase their body width to reach a size-refuge. We found that increased temperatures increased predation rates, although this was counteracted by high basal resource availability, which further decreased salamander growth. Surprisingly, salamanders caused tadpoles to grow larger and express more extreme defensive phenotypes as resource levels decreased under warming, most likely due to their increased risk of predation. Thus, temperature and resources influenced defensive phenotype expression and its impacts on predator and prey growth by affecting their interaction strength. Our results indicate that basal resource levels can modify the impacts of increased temperatures on predator-prey interactions and its consequences for food webs.
  • Kunio Takatsu, Osamu Kishida
    ECOLOGY 96 (7) 1887 - 1898 0012-9658 2015/07 [Refereed][Not invited]
     
    Although natural populations consist of individuals with different traits, and the degree of phenotypic variation varies among populations, the impact of phenotypic variation on ecological interactions has received little attention, because traditional approaches to community ecology assume homogeneity of individuals within a population. Stage structure, which is a common way of generating size and developmental variation within predator populations, can drive cannibalistic interactions, which can affect the strength of predatory effects on the predator's heterospecific prey. Studies have shown that predator cannibalism weakens predatory effects on heterospecific prey by reducing the size of the predator population and by inducing less feeding activity of noncannibal predators. We predict, however, that predator cannibalism, by promoting rapid growth of the cannibals, can also intensify predation pressure on heterospecific prey, because large predators have large resource requirements and may utilize a wider variety of prey species. To test this hypothesis, we conducted an experiment in which we created carnivorous salamander (Hynobius retardatus) populations with different stage structures by manipulating the salamander's hatch timing (i.e., populations with large or small variation in the timing of hatching), and explored the resultant impacts on the abundance, behavior, morphology, and life history of the salamander's large heterospecific prey, Rana pirica frog tadpoles. Cannibalism was rare in salamander populations having small hatch-timing variation, but was frequent in those having large hatch-timing variation. Thus, giant salamander cannibals occurred only in the latter. We clearly showed that salamander giants exerted strong predation pressure on frog tadpoles, which induced large behavioral and morphological defenses in the tadpoles and caused them to metamorphose late at large size. Hence, predator cannibalism arising from large variation in the timing of hatching can strengthen predatory effects on heterospecific prey and can have impacts on various traits of both predator and prey. Because animals commonly broaden their diet as they grow, such negative impacts of predator cannibalism on the heterospecific prey may be common in interactions between predators and prey species of similar size.
  • Masatoshi Matsunami, Jun Kitano, Osamu Kishida, Hirofumi Michimae, Toru Miura, Kinya Nishimura
    MOLECULAR ECOLOGY 24 (12) 3064 - 3076 0962-1083 2015/06 [Refereed][Not invited]
     
    Predator- and prey-induced phenotypic plasticity is widely observed among amphibian species. Although ecological factors inducing diverse phenotypic responses have been extensively characterized, we know little about the molecular bases of variation in phenotypic plasticity. Larvae of the Hokkaido salamander, Hynobius retardatus, exhibit two distinct morphs: the presence of their prey, Rana pirica tadpoles, induces a broad-headed attack morph, and the presence of predatory dragonfly nymphs (Aeshna nigroflava) induces a defence morph with enlarged external gills and a high tail. To compare the genes involved in predator- and prey-induced phenotypic plasticity, we carried out a de novo transcriptome analysis of Hokkaido salamander larvae exposed to either prey or predator individuals. First, we found that the number of genes involved in the expression of the defence morph was approximately five times the number involved in the expression of the attack morph. This result is consistent with the fact that the predator-induced plasticity involves more drastic morphological changes than the prey-induced plasticity. Second, we found that particular sets of genes were upregulated during the induction of both the attack and defence morphs, but others were specific to the expression of one or the other morph. Because both shared and unique molecular mechanisms were used in the expression of each morph, the evolution of a new plastic phenotype might involve both the co-option of pre-existing molecular mechanisms and the acquisition of novel regulatory mechanisms.
  • Tsukasa Mori, Yukio Yanagisawa, Yoichiro Kitani, Manabu Sugiyama, Osamu Kishida, Kinya Nishimura
    BMC GENOMICS 16 258  1471-2164 2015/04 [Refereed][Not invited]
     
    Background: Rana pirica tadpoles show morphological changes in response to a predation threat: larvae of the dragonfly Aeshna nigroflava induce heightened tail depth, whereas larval salamander Hynobius retardatus induce a bulgy morphology with heightened tail depth. Although both predators induce similar tail morphologies, it is possible that there are functional differences between these tail morphs. Results: Here, we performed a discriminant microarray analysis using Xenopus laevis genome arrays to compare tail tissues of control and predator-exposed tadpoles. We identified 9 genes showing large-scale changes in their expression profile: ELAV-like1, methyltransferase like 7A, dolichyl-phosphate mannosyltransferase, laminin subunit beta-1, gremlin 1, BCL6 corepressor-like 1, and three genes of unknown identity. A further 80 genes showed greater than 5 fold differences in expression after exposure to dragonfly larvae and 81 genes showed altered expression after exposure to larval salamanders. Predation-threat responsive genes were identified by selecting genes that reverted to control levels of expression following removal of the predator. Thirteen genes were induced specifically by dragonfly larvae, nine others were salamander-specific, and sixteen were induced by both. Functional analyses indicated that some of the genes induced by dragonfly larvae caused an increase in laminins necessary for cell adhesion in the extracellular matrix. The higher expression of gremlin 1 and HIF1a genes after exposure to dragonfly larvae indicated an in vivo hypoxic reaction, while down-regulation of syndecan-2 may indicate impairment of angiogenesis. Exposure to larval salamanders caused down-regulation of XCIRP-1, which is known to inhibit expression of adhesion molecules; the tadpoles showed reduced expression of ca(E)-catenin, small muscle protein, dystrophin, and myosin light chain genes. Conclusion: The connective tissue of tadpoles exposed to larval salamanders may be looser. The differences in gene expression profiles induced by the two predators suggest that there are functional differences between the altered tail tissues of the two groups of tadpoles.
  • Osamu Kishida, Ayumi Tezuka, Akiko Ikeda, Kunio Takatsu, Hirofumi Michimae
    Functional Ecology 29 (4) 469 - 478 0269-8463 2015/04 [Refereed][Not invited]
     
    In most animal species, the hatchling stage is a highly vulnerable life-history stage. In many fish and amphibian species, hatchling abundance varies substantially among sites and years, with the result that selection strength in conspecific interactions such as cannibalism is also variable. The variability of selection leads species to evolve phenotypic plasticity, and adaptive trait changes in hatchlings that depend on the density of conspecifics can therefore be expected. However, plasticity strategies in response to cannibalistic interactions in this vulnerable life-history stage have received little attention. Because cannibalism success is dependent on the size balance between predator capturing organ and prey body, and also on the prey-capturing ability of the cannibal and the escape ability of its prey, we hypothesize that hatchlings will exhibit faster growth and development in response to conspecific interactions. We performed a series of experiments to test this hypothesis, using pre-feeding larvae of a cannibalistic salamander (Hynobius retardatus). Many traits of the hatchlings reared with conspecifics were larger than the same traits in those reared alone, because the former hatchlings grew faster and were more advanced developmentally. The time to the beginning of feeding was shorter, and swimming speed as an indicator of escape performance was faster, for hatchlings reared with conspecifics. Hatchlings reared with conspecifics more successfully cannibalized small hatchlings and were also highly resistant to being cannibalized by large conspecifics, compared with hatchlings reared alone. These differences in cannibalism success and avoidance of cannibalization were well explained by differences in gape and head size, respectively, between the interacting hatchlings. Therefore, acceleration of growth and development of hatchlings in the proximate presence of conspecifics may confer significant fitness advantages on hatchlings in a high-density cannibalistic situation. Developmental and growth plasticity may thus be a powerful adaptive mechanism that allows individuals to respond to the dynamic character of salamander populations in nature.
  • Megumi Nosaka, Noboru Katayama, Osamu Kishida
    OIKOS 124 (2) 225 - 234 0030-1299 2015/02 [Refereed][Not invited]
     
    In many size-dependent predator-prey systems, hatching phenology strongly affects predator-prey interaction outcomes. Early-hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator-prey interaction outcomes over the whole interaction period because the predator-prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator-prey interactions via a feedback mechanism between the predator-prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator-prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator-prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early-hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator-superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early-hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator-superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short-term population dynamics and life history of the prey. Because consumption of large nutrient-rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size-dependent trophic relationships.
  • Allometric equations for estimation of energy contents from body length for common amphibians (Hynobius retardatus and Rana pirica) in Hokkaido, Japan
    Kunio Takatsu, Osamu Kishida
    Herpetology Notes 8 187 - 191 2015 [Refereed][Not invited]
  • Maricar Aguilos, Kentaro Takagi, Naishen Liang, Masahito Ueyama, Karibu Fukuzawa, Mutsumi Nomura, Osamu Kishida, Tatsuya Fukazawa, Hiroyuki Takahashi, Chikara Kotsuka, Rei Sakai, Kinya Ito, Yoko Watanabe, Yasumi Fujinuma, Yoshiyuki Takahashi, Takeshi Murayama, Nobuko Saigusa, Kaichiro Sasa
    Agricultural and Forest Meteorology 197 26 - 39 0168-1923 2014/10 [Refereed]
  • Noboru Katayama, Alessandro O. Silva, Osamu Kishida, Masayuki Ushio, Satoshi Kita, Takayuki Ohgushi
    ECOLOGICAL ENTOMOLOGY 39 (4) 511 - 518 0307-6946 2014/08 [Refereed][Not invited]
     
    1. Plants take nutrients from the rhizosphere via two pathways: (i) by absorbing soil nutrients directly via their roots and (n) indirectly via symbiotic associations with nutrient-providing microbes. Herbivorous insects can alter these pathways by herbivory, adding their excrement to the soil, and affecting plant microbe associations. 2. Little is known, however, about the effects of herbivorous insects on plant nutrient uptake. Greenhouse experiments with soybean, aphids, and rhizobia were carried out to examine the effects of aphids on plant nutrient uptake. 3. First, the inorganic soil nitrogen and the sugar in aphid honeydew between aphid-infected and -free plants were compared. It was found that aphid honeydew added 41 g M-2 of sugar to the soil, and that aphids decreased the inorganic soil nitrogen by 86%. This decrease may have been caused by microbial immobilisation of soil nitrogen followed by increased microbial abundance as a result of aphid honeydew, 4. Second, nitrogen forms in xylem sap between aphid-infected and -free plants were compared to examine nitrogen uptake. Aphids decreased the nitrogen uptake via both pathways, and strength of the impact on direct uptake via plant roots was greater than indirect uptake via rhizobia. The reduced nitrogen uptake by the direct pathway was as a result of microbial immobilisation, and that by the indirect pathway was probably because of the interaction of microbial immobilisation and carbon stress, which was caused by aphid infection, 5. The present results demonstrate that herbivorous insects can negatively influence the two pathways of plant nutrient uptake and alter their relative importance.
  • Osamu Kishida, Zacharia Costa, Ayumi Tezuka, Hirofumi Michimae
    JOURNAL OF ANIMAL ECOLOGY 83 (4) 899 - 906 0021-8790 2014/07 [Refereed][Not invited]
     
    Phenotypic plasticity can have strong impacts on predator-prey interactions. Although much work has examined the effects of inducible defences, less understood is how inducible offences in predators affect predator-prey interactions and predator and prey phenotypes. Here, we examine the impacts of an inducible offence on the interactions and life histories of a cohort of predatory Hynobius retardatus salamander larvae and their prey, Rana pirica tadpoles. We examined larval (duration, survival) and post-metamorphic (size) traits of both species after manipulating the presence/absence of tadpoles and salamanders with offensive (broadened gape width) or non-offensive phenotypes in pond enclosures. Offensive phenotype salamanders reduced tadpole survival and metamorph emergence by 58% compared to tadpole-only treatments, and by over 30% compared to non-offensive phenotypes. Average time to metamorphosis of frogs was delayed by 30% in the presence of salamanders, although this was independent of salamander phenotype. Thus, offensive phenotype salamanders reduced the number of tadpoles remaining in the pond over time by reducing tadpole survival, not by altering patterns of metamorph emergence. Offensive phenotypes also caused tadpoles to metamorphose 19% larger than no salamander treatments and 6% larger than non-offensive phenotype treatments. Pooled across salamander treatments, tadpoles caused salamanders to reach metamorphosis faster and larger. Moreover, in the presence of tadpoles, offensive phenotype salamanders metamorphosed 25% faster and 5% larger than non-offensive phenotype salamanders, but in their absence, neither their size nor larval period differed from non-offensive phenotype individuals. To our knowledge, this study is the first to demonstrate that inducible offences in predators can have strong impacts on predator and prey phenotypes across multiple life stages. Since early metamorphosis at a larger size has potential fitness advantages, the impacts of offensive phenotypes on frog and salamander life histories likely have significant consequences for individuals and populations. Furthermore, increased predation on tadpoles likely causes offensive phenotype individuals to have strong impacts on pond communities. Future studies should examine the fitness consequences of morphological and life-history plasticity across multiple life stages and should address the population and community level consequences of offensive phenotypes.
  • Hirofumi Michimae, Ayumi Tezuka, Takeshi Emura, Osamu Kishida
    EVOLUTIONARY ECOLOGY RESEARCH 16 (7) 617 - 629 1522-0613 2014 [Refereed][Not invited]
     
    Background: Fitness trade-offs of plastic traits between alternative environments are a prerequisite for the evolution of phenotypic plasticity; however, the costs associated with plastic traits have yet to be determined. Most empirical studies have assessed the costs of plastic traits by investigating just two environments (to elicit plasticity), and only one or two environments to evaluate the consequences of plasticity. In contrast, in nature, organisms are constantly subjected to multiple environments, and the expression and magnitude of the costs of plastic traits are occasionally context-dependent. Objective: Analyse the costs of plastic traits across multiple environments. Methods: We determined the benefits and costs of two plastic responses (predator-and prey-induced morphologies) of larvae of the salamander Hynobius retardatus to larval survival, time to metamorphosis, and body size at metamorphosis in three different environments [using tadpoles of an anuran frog as prey, larvae of a predatory dragonfly, or no change agent (conspecific larvae only)]. Results: The benefits of the alternative phenotypes were evident in the two inducing environments, but the costs were greater or more easily detected in crossover environments. The trade-offs appeared in combinations in the crossover environments, and thus were context-dependent. Conclusions: The cross-environmental costs of plastic traits are necessary for the evolution of phenotypic plasticity. Our findings highlight the importance of measuring the costs and benefits of plastic traits across multiple environments.
  • Noboru Katayama, Alessandro Oliveria Silva, Osamu Kishida, Takayuki Ohgushi
    ECOLOGICAL ENTOMOLOGY 38 (6) 627 - 630 0307-6946 2013/12 [Refereed][Not invited]
     
    Herbivorous insects may have significant impacts on litter decomposition through modification of plant litter quality and quantity. The effects of herbivorous insects on decomposition processes are of growing interest. Here, experiments were conducted to examine how sap-feeding aphids modify plant litter and whether the aphid-induced modification influences litter decomposition processes, using a plant-herbivore system consisting of soybean [Glycine max (L.)] and soybean aphids (Aphis glycines Matsumura). First, litter traits produced by aphid-free and aphid-infected plants were compared, and it was found that aphids did not affect litter mass and carbon concentration, but significantly decreased the nitrogen concentration. Such aphid-mediated modification of litter quality may cause deceleration of litter decomposition as the higher C/N ratio inhibits litter decomposition. A decomposition experiment was then carried out to compare the decomposition of litter between the aphid-free and aphid-infected plants. No impacts of aphid herbivory were found on litter carbon mineralisation but negative impacts were found on nitrogen mineralisation. Litter nitrogen mineralisation of aphid-infected plants decreased by 40% and 28% compared with that of aphid-free plants 1 and 3months after commencement of the experiment, respectively. The experimental results clearly showed that aphids decelerated litter nitrogen mineralisation by modifying litter quality.
  • Mitsuru Hattori, Osamu Kishida, Takao Itino
    EVOLUTIONARY ECOLOGY 27 (5) 847 - 862 0269-7653 2013/09 [Refereed][Not invited]
     
    Eusocial aphids produce sterile individuals ("soldiers") that specialize behaviorally and morphologically to protect their colony from predators, while production of soldiers can negatively affect colony growth because of reproductive allocation and opportunity cost. Hence, a cost-saving soldier production strategy is expected to be favored. Here, we hypothesize that, to save the cost, a eusocial aphid Ceratovacuna japonica produces soldiers with smaller weapon in the season when predators are not abundant. The abundance of two specialist lepidopteran predators (i.e., Taraka hamada and Atkinsonia ignipicta) of C. japonica dramatically increased, and aphid colony size significantly decreased, from July to August. In line with these, the soldiers in August had larger weapons (i.e., frontal horns) than those in June, indicating a correlational increase in weapon size with predation pressure. We predict that a reliable prospective signal indicating the coming of midsummer (environmental temperature) induces mother aphids to produce soldiers with larger weapons. Experiments clarified that soldiers produced at 20 A degrees C (typical temperature of July to August) had larger weapons than those produced at 15 A degrees C (typical temperature of May to July). Such phenotypic plasticity appears to be adaptive to maximize the fitness of C. japonica under a temporally variable but predictable predation environment. These results indicate that C. japonica aphids not merely have distinctive reproductive-and soldier castes, but also produce differentially armed soldiers in a habitat with temporally changing predation risks.
  • Overwintered Hynobius retardatus salamander larvae can induce defensive bulgy morph in Rana pirica tadpoles
    Kishida O, Tezuka A
    Herpetology Notes 6 183 - 185 2013/03 [Refereed][Not invited]
  • Kunio Takatsu, Osamu Kishida
    Evolutionary Ecology 27 (1) 1 - 11 0269-7653 2013/01 [Refereed][Not invited]
     
    Inducible defenses of prey and inducible offenses of predators are examples of adaptive phenotypic plasticity. Although evolutionary ecologists have paid considerable attention to the adaptive significances of these strategies, they have rarely focused on their evolutionary impacts on the interacting species. Because the functional phenotypes of predator and prey determine strength of interactions between the species, the inducible plasticity can modify selective pressure on trait distribution and, ultimately, trait evolution in the interacting species. We experimentally tested this hypothesis in a predator-prey system composed of salamander larvae (Hynobius retardatus) and frog tadpoles (Rana pirica) capable of expressing antagonistic inducible offensive or defensive traits, an enlarged gape in the salamander larvae and a bulgy body in the tadpoles, when predator-prey interactions are strong. We examined selection strength on the tadpole's defensive trait by comparing survival rates of tadpoles with different defensive levels under predation pressure from offensive or non-offensive salamander larvae. Survival rates of more-defensive tadpoles were greater than those of less-defensive tadpoles only when the tadpoles were exposed to offensive salamander larvae; thus, the predator's offensive phenotype could select for an amplified defensive phenotype in their prey. As the expression of inducible offenses by H. retardatus larvae depends greatly on the composition of its ecological community, the inducible defensive bulgy morph of R. pirica tadpoles might have evolved in response to the variable expression of the H. retardatus offensive larval phenotype.
  • M. Hattori, O. Kishida, T. Itino
    Insectes Sociaux 60 15 - 21 0020-1812 2013/01 [Refereed][Not invited]
     
    Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species' natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator's body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers' colony mates time to reproduce or to escape from the predator. © 2012 International Union for the Study of Social Insects (IUSSI).
  • Tsukasa Mori, Yoichiro Kitani, Jun Ogihara, Manabu Sugiyama, Goshi Yamamoto, Osamu Kishida, Kinya Nishimura
    BIOLOGY OPEN 1 (4) 308 - 317 2046-6390 2012/04 [Refereed][Not invited]
     
    The rapid induction of a defensive morphology by a prey species in face of a predation risk is an intriguing in ecological context; however, the physiological mechanisms that underlie this phenotypic plasticity remain uncertain. Here we investigated the phenotypic changes shown by Rana pirica tadpoles in response to a predation threat by larvae of the salamander Hynobius retardatus. One such response is the bulgy morph phenotype, a relatively rapid swelling in size by the tadpoles that begins within 4 days and reaches a maximum at 8 to 10 days. We found that although the total volume of bodily fluid increased significantly (P<0.01) in bulgy morph tadpoles, osmotic pressure was maintained at the same level as control tadpoles by a significant increase (P<0.01) in Na and Cl ion concentrations. In our previous report, we identified a novel frog gene named pirica that affects the waterproofing of the skin membrane in tadpoles. Our results support the hypothesis that predator-induced expression of pirica on the skin membrane causes retention of absorbed water. Midline sections of bulgy morph tadpoles showed the presence of swollen connective tissue beneath the skin that was sparsely composed of cells containing hyaluronic acid. Mass spectrographic (LC-MS/MS) analysis identified histone H3 and 14-3-3 zeta as the most abundant constituents in the liquid aspirated from the connective tissue of bulgy tadpoles. Immunohistochemistry using antibodies against these proteins showed the presence of non-chromatin associated histone H3 in the swollen connective tissue. Histones and 14-3-3 proteins are also involved in antimicrobial activity and secretion of antibacterial proteins, respectively. Bulgy tadpoles have a larger surface area than controls, and their skin often has bite wounds inflicted by the larval salamanders. Thus, formation of the bulgy morph may also require and be supported by activation of innate immune systems. (C) 2012. Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Share Alike License (http://creativecommons.org/licenses/by-nc-sa/3.0).
  • Osamu Kishida, Geoffrey C. Trussell, Ayaka Ohno, Shinya Kuwano, Takuya Ikawa, Kinya Nishimura
    JOURNAL OF ANIMAL ECOLOGY 80 (6) 1278 - 1287 0021-8790 2011/11 [Refereed][Not invited]
     
    1. Cannibalism can play a prominent role in the structuring and dynamics of ecological communities. Previous studies have emphasized the importance of size structure and density of cannibalistic species in shaping short- and long-term cannibalism dynamics, but our understanding of how predators influence cannibalism dynamics is limited. This is despite widespread evidence that many prey species exhibit behavioural and morphological adaptations in response to predation risk. 2. This study examined how the presence and absence of predation risk from larval dragonflies Aeshna nigroflava affected cannibalism dynamics in its prey larval salamanders Hynobius retardatus. 3. We found that feedback dynamics between size structure and cannibalism depended on whether dragonfly predation risk was present. In the absence of dragonfly risk cues, a positive feedback between salamander size structure and cannibalism through time occurred because most of the replicates in this treatment contained at least one salamander larvae having an enlarged gape (i.e. cannibal). In contrast, this feedback and the emergence of cannibalism were rarely observed in the presence of the dragonfly risk cues. Once salamander size divergence occurred, experimental reversals of the presence or absence of dragonfly risk cues did not alter existing cannibalism dynamics as the experiment progressed. Thus, the effects of risk on the mechanisms driving cannibalism dynamics likely operated during the early developmental period of the salamander larvae. 4. The effects of dragonfly predation risk on behavioural aspects of cannibalistic interactions among hatchlings may prohibit the initiation of dynamics between size structure and cannibalism. Our predation trials clearly showed that encounter rates among hatchlings and biting and ingestion rates of prospective prey by prospective cannibals were significantly lower in the presence vs. absence of dragonfly predation risk even though the size asymmetry between cannibals and victims was similar in both risk treatments. These results suggest that dragonfly risk cues first suppress cannibalism among hatchlings and then prevent size variation from increasing through time. 5. We suggest that the positive feedback dynamics between size structure and cannibalism and their modification by predation risk may also operate in other systems to shape the population dynamics of cannibalistic prey species as well as overall community dynamics.
  • Akihiko Mougi, Osamu Kishida, Yoh Iwasa
    EVOLUTION 65 (4) 1079 - 1087 0014-3820 2011/04 [Refereed][Not invited]
     
    Inducible defenses of prey and inducible offenses of predators are drastic phenotypic changes activated by the interaction between a prey and predator. Inducible defenses occur in many taxa and occur more frequently than inducible offenses. Recent empirical studies have reported reciprocal phenotypic changes in both predator and prey. Here, we model the coevolution of inducible plasticity in both prey and predator, and examine how the evolutionary dynamics of inducible plasticity affect the population dynamics of a predator-prey system. Under a broad range of parameter values, the proportion of predators with an offensive phenotype is smaller than the proportion of prey with a defensive phenotype, and the offense level is relatively lower than the defense level at evolutionary end points. Our model also predicts that inducible plasticity evolves in both species when predation success depends sensitively on the difference in the inducible trait value between the two species. Reciprocal phenotypic plasticity may be widespread in nature but may have been overlooked by field studies because offensive phenotypes are rare and inconspicuous.
  • Shunsuke Utsumi, Osamu Kishida, Takayuki Ohgushi
    POPULATION ECOLOGY 52 (4) 457 - 459 1438-3896 2010/10 [Refereed][Not invited]
  • Osamu Kishida, Geoffrey C. Trussell, Akihiko Mougi, Kinya Nishimura
    POPULATION ECOLOGY 52 (1) 37 - 46 1438-3896 2010/01 [Refereed][Not invited]
     
    The outcome of species interactions is often strongly influenced by variation in the functional traits of the individuals participating. A rather large body of work demonstrates that inducible morphological plasticity in predators and prey can both influence and be influenced by species interaction strength, with important consequences for individual fitness. Much of the past research in this area has focused on the ecological and evolutionary significance of trait plasticity by studying single predator-prey pairs and testing the performance of individuals having induced and noninduced phenotypes. This research has thus been critical in improving our understanding of the adaptive value of trait plasticity and its widespread occurrence across species and community types. More recently, researchers have expanded this foundation by examining how the complexity of organismal design and community-level properties can shape plasticity in functional traits. In addition, researchers have begun to merge evolutionary and ecological perspectives by linking trait plasticity to community dynamics, with particular attention on trait-mediated indirect interactions. Here, we review recent studies on inducible morphological plasticity in predators and their prey with an emphasis on internal and external constraints and how the nature of predator-prey interactions influences the expression of inducible phenotypes. In particular, we focus on multiple-trait plasticity, flexibility and modification of inducible plasticity, and reciprocal plasticity between predator and prey. Based on our arguments on these issues, we propose future research directions that should better integrate evolutionary and population studies and thus improve our understanding of the role of phenotypic plasticity in predator-prey population and community dynamics.
  • Osamu Kishida, Geoffrey C. Trussell, Kinya Nishimura, Takayuki Ohgushi
    ECOLOGY 90 (11) 3150 - 3158 0012-9658 2009/11 [Refereed][Not invited]
     
    Trophic cascades are often a potent force in ecological communities, but abiotic and biotic heterogeneity can diffuse their influence. For example, inducible defenses in many species create variation in prey edibility, and size-structured interactions, such as cannibalism, can shift predator diets away from heterospecific prey. Although both factors diffuse cascade strength by adding heterogeneity to trophic interactions, the consequences of their interaction remain poorly understood. We show that inducible defenses in tadpole prey greatly intensify cannibalism in predatory larval salamanders. The likelihood of cannibalism was also strongly influenced by asymmetries in salamander size that appear to be most important in the presence of defended prey. Hence, variation in prey edibility and the size structure of the predator may synergistically affect predator-prey population dynamics by reducing prey mortality and increasing predator mortality via cannibalism. We also suggest that the indirect effects of prey defenses may shape the evolution of predator traits that determine diet breadth and how trophic dynamics unfold in natural systems.
  • Akihiko Mougi, Osamu Kishida
    JOURNAL OF ANIMAL ECOLOGY 78 (6) 1172 - 1181 0021-8790 2009/11 [Refereed][Not invited]
     
    P>1. Inducible defences of prey and inducible offences of predators are prevalent strategies in trophic interactions with temporal variation. Due to the inducible properties of the functional traits themselves, which drive the dynamic predator-prey relationship on an ecological time-scale, predator and prey may reciprocally interact through their inducible traits (i.e. reciprocal phenotypic plasticity). 2. Although overwhelming evidence of the stabilizing effect of inducible traits in either species on community dynamics forcefully suggests a critical ecological role for reciprocal plasticity in predator-prey population dynamics, our understanding of its ecological consequences is very limited. 3. Within a mathematical modelling framework, we investigated how reciprocal plasticity influences the stability of predator-prey systems. 4. By assuming two types of phenotypic shift, a density-dependent shift and an adaptive phenotypic shift, we examined two interaction scenarios with reciprocal plasticity: (i) an arms-race-like relationship, in which the defensive prey phenotype is more protective against both predator phenotypes (i.e. normal and offensive) than the normal prey phenotype, and the offensive predator is a more efficient consumer, preying upon both prey phenotypes (i.e. normal and defensive), than the normal predator and (ii) a matching response-like relationship, in which the offensive predator consumes more defensive prey and fewer normal prey than the normal predator. 5. Results of both phenotypic shift models consistently suggest that given the used set of parameter values, the arms-race-like reciprocal plasticity scenario has the largest stability area, when compared with the other scenarios. In particular, higher stability is achieved when the prey exhibits a high-performance inducible defence. Furthermore, this stabilization is so strong that the destabilizing effects of enrichment may be eliminated, even though the higher flexibility of plasticity does not always stabilize a system. 6. Recent empirical studies support our model predictions. Clear-cut examples of reciprocal phenotypic plasticity show an arms-race-like relationship in which prey species exhibit induced high-performance defences. We may need to re-examine reported predator-prey interactions in which predator or prey exhibits inducible plasticity to determine whether arms-race-like reciprocal plasticity is a general ecological phenomenon.
  • Tsukasa Mori, Hiroko Kawachi, Chiharu Imai, Manabu Sugiyama, Youichi Kurata, Osamu Kishida, Kinya Nishimura
    PLOS ONE 4 (6) e5936  1932-6203 2009/06 [Refereed][Not invited]
     
    Tadpoles of the anuran species Rana pirica can undergo predator-specific morphological responses. Exposure to a predation threat by larvae of the salamander Hynobius retardatus results in formation of a bulgy body (bulgy morph) with a higher tail. The tadpoles revert to a normal phenotype upon removal of the larval salamander threat. Although predator-induced phenotypic plasticity is of major interest to evolutionary ecologists, the molecular and physiological mechanisms that control this response have yet to be elucidated. In a previous study, we identified various genes that are expressed in the skin of the bulgy morph. However, it proved difficult to determine which of these were key genes in the control of gene expression associated with the bulgy phenotype. Here, we show that a novel gene plays an important role in the phenotypic plasticity producing the bulgy morph. A functional microarray analysis using facial tissue samples of control and bulgy morph tadpoles identified candidate functional genes for predator-specific morphological responses. A larger functional microarray was prepared than in the previous study and used to analyze mRNAs extracted from facial and brain tissues of tadpoles from induction-reversion experiments. We found that a novel uromodulin-like gene, which we name here pirica, was up-regulated and that keratin genes were down-regulated as the period of exposure to larval salamanders increased. Pirica consists of a 1296 bp open reading frame, which is putatively translated into a protein of 432 amino acids. The protein contains a zona pellucida domain similar to that of proteins that function to control water permeability. We found that the gene was expressed in the superficial epidermis of the tadpole skin.
  • Osamu Kishida, Geoffrey C. Trussell, Kinya Nishimura
    ECOLOGY 90 (5) 1217 - 1226 0012-9658 2009/05 [Refereed][Not invited]
     
    Antagonistic phenotypic plasticity may strongly influence trait evolution in tightly interacting predator-prey pairs as well as the role that trait plasticity plays in community dynamics. Most work on trait plasticity has focused on single predator-prey pairs, but prey must often contend with multiple predators in natural environments. Hence, a better understanding of the evolutionary and ecological significance of phenotypic plasticity requires experiments that examine how multiple predators shape prey trait plasticity. Here, using a simple food chain consisting of a top predator (dragonfly larvae, Aeshna nigroflava), an intermediate predator (salamander larvae, Hynobius retardatus), and frog (Rana pirica) tadpoles as prey, we show that the presence of dragonfly risk cues substantially modifies the intensity of antagonistic morphological plasticity in both amphibians. In the absence of dragonflies, tadpoles produced bulgier bodies in response to salamanders, and salamanders responded to this defense by enlarging their gape size. However, in the presence of dragonfly risk cues, the expression of both antagonistic traits was significantly reduced because tadpoles and salamanders produced phenotypes that are more effective against dragonfly predators. Thus, the reduced antagonism likely emerged, in part, because the benefits of antagonistic trait expression were outweighed by the potential cost of increased vulnerability to dragonfly predation. In addition, our results suggest that when all three species were present, salamander activity levels, which influence the amount of signals required to induce antagonistic traits, were more strongly affected by dragonfly risk cues than were tadpole activity levels. This species-specific difference in activity levels was likely responsible for the reduced tadpole mortality caused by salamanders in the presence vs. absence of dragonfly risk cues. Hence, dragonflies had a positive trait-mediated indirect effect on tadpoles by modifying both the morphological and behavioral traits of salamanders.
  • Tadashi Iwami, Osamu Kishida, Kinya Nishimura
    PLOS ONE 2 (10) e1084  1932-6203 2007/10 [Refereed][Not invited]
     
    Organisms often exhibit phenotypic plasticity in multiple traits in response to impending environmental change. Multiple traits phenotypic plasticity is complex syndrome brought on by causal relations in ecological and physiological context. Larvae of the salamander Hynobius retardatus exhibit inducible phenotypic plasticity of two traits, when at risk of predation by dragonfly larvae. One induced phenotype is an adaptive defense behaviour, i.e., stasis at the bottom of water column, directly triggered by the predation risk. Another one is a compensatory phenotype, i.e., enlarged external gills, for an unavoidable cost (hypoxia) associated with the induced defense. We identified two ways by which this compensatory phenotype could be induced. The compensatory phenotype is induced in response to not only the associated hypoxic conditions resulting from the induced defense but also the most primary but indirect cause, presence of the predator.
  • Osamu Kishida, Geoffrey C. Trussell, Kinya Nishimura
    ECOLOGY 88 (8) 1948 - 1954 0012-9658 2007/08 [Refereed][Not invited]
     
    Predator-induced morphological defenses are a well-known form of phenotypic plasticity, but we continue to have a limited understanding of geographic variation in these responses and its genetic basis. Here we examine genetic variation and geographic differentiation in the inducible defenses of tadpoles (Rana pirica) in response to predatory salamander larvae (Hynobius retardatus). To do so, we crossed male and female frogs from a "mainland" Japanese island having predaceous salamanders and a more isolated island not having predaceous salamanders and raised resulting offspring in the presence and absence of H. retardatus. Mainland tadpoles exhibited a higher capacity to express the inducible morphology (a more bulgy body) than those from the predator-free island, and expression of the bulgy morph in mainland-island hybrids produced phenotypes that were intermediate to those produced by pure crosses. In addition, parental sex had no effect on expression of the bulgy morph. Our results support the hypothesis that geographic variation in inducible defenses is linked to the additive effects of autosomal alleles that are shaped by differences in historical exposure to the inducing predator.
  • Kishida Osamu, Nishimura Kinya
    Japanese Journal of Ecology 日本生態学会 57 (1) 40 - 47 0021-5007 2007/03/31 [Refereed][Not invited]
     
    多くの動物は、捕食者に出会うと逃げたり隠れたりするが、形さえも変化させ捕食を回避しようとするものもいる。形態の変化による防御戦略は誘導防御形態戦略とよばれ、多様な生物分類群でみられる表現型可塑性として知られる。最近の研究では、捕食者動物は、ただ捕食されにくい形に変わるだけでなく、その変化が柔軟であり、捕食者環境の時間的・空間的な変異によく対応していることが知られている。本稿では、エゾアカガエルのオタマジャクシの捕食者誘導形態の防御機能と、柔軟な形態変化能について紹介する。エゾアカガエルのオタマジャクシは、捕食者のエゾサンショウウオの幼生とオオルリボシヤンマのヤゴに対して、それぞれに特異的な形態を発現する。サンショウウオ幼生によって誘導された膨満型の形態はサンショウウオ幼生による丸のみを妨げ、ヤゴによって誘導された高尾型の形態はヤゴによる捕食を回避するために有効である。これらの形態変化は柔軟性に富んでおり、一度、どちらかの捕食者に対して特異的な防御形態を発現した後でも、捕食者が交替したときには、新たな捕食者に特異的な防御形態へ変化できる。また、捕食の危険が取り除かれたときは元の形態へと戻る。捕食者特異的な形態の互換性は、捕食者種に特異的な防御形態誘導を獲得するうえで重要な役割を果たしたと考えられる。また、形態変化の可逆性は防御にコストがかかることを示唆している。これらの形態変化...
  • Osamu Kishida, Yuuki Mizuta, Kinya Nishimura
    ECOLOGY 87 (6) 1599 - 1604 0012-9658 2006/06 [Refereed][Not invited]
     
    In biological interactions, phenotypic change in interacting organisms induced by their interaction partners causes a substantial shift in some environmental factor of the partners, which may subsequently change their phenotype in response to that modified environmental factor. Few examples of such arms-race-like plastic responses, known as reciprocal phenotypic plasticity, have been identified in predator - prey interactions. We experimentally identified a reciprocal defensive plastic response of a prey species against a predator with a predaceous phenotype using a model system of close predator - prey interaction. Rana pirica tadpoles ( the prey species) were reared with larvae of the salamander Hynobius retardatus ( the predator species) having either a predaceous or a typical, nonpredaceous phenotype. The H. retardatus larvae with the predaceous phenotype, which is known to be induced by the presence of R. pirica tadpoles, induced a more defensive phenotype in the tadpoles than did larvae with the typical phenotype. The result suggests that the reciprocal phenotypic plasticity of R. pirica tadpoles is in response to a phenotype-specific signal under a close-signal recognition process.
  • O Kishida, K Nishimura
    Journal of Animal Ecology 75 (3) 705 - 712 0021-8790 2006/05 [Refereed][Not invited]
     
    Predator-induced morphological defences are produced in response to an emergent predator regime. In natural systems, prey organisms usually experience temporal shifting of the composition of the predator assemblage and of the intensity of predation risk from each predator species. Although, a repetitive morphological change in response to a sequential shift of the predator regime such as alteration of the predator species or diminution of the predation risk may be adaptive, such flexible inducible morphological defences are not ubiquitous. We experimentally addressed whether a flexible inducible morphological defence is accomplished in response to serial changes in the predation regime, using a model prey species which adopt different defensive morphological phenotypes in response to different predator species. Rana pirica (Matsui) tadpoles increased body depth and tail depth against the predatory larval salamander Hynobius retardatus (Dunn); on the other hand, they only increased tail depth against the predatory larval dragonfly Aeshna nigroflava (Martin). Rana pirica tadpoles with the predator-specific phenotypes were subjected to removal or exchange of the predator species. After removal of the predator species, tadpoles with each predator-specific phenotype changed their phenotype to the nondefensive basic one, suggesting that both predator-specific phenotypes are costly to maintain. After an exchange of the predator species, tadpoles with each predator-specific phenotype reciprocally, flexibly shifted their phenotype to the now more suitable predator-specific one only by modifying their body part. The partial modification can effectively reduce time and energy expenditures involved in repetitive morphological changes, and therefore suggest that the costs of the flexible morphological changes are reduced.
  • Osamu Kishida, Kinya Nishimura
    Evolutionary Ecology Research 7 (4) 619 - 631 1522-0613 2005/05 [Refereed][Not invited]
     
    Question: What conditions are required for evolution of predator-specific inducible defences? Hypotheses: (1) Prey organisms distinguish among predators to which they are exposed. (2). P Prey individuals with a predator-specific defence must attain higher survivorship than those with a mismatched defensive phenotype. Organisms: Prey, anuran tadpoles (Rana pirica); biting type predator, dragonfly larvae (Aeshna nigroflava); swallowing type predator, salamander larvae (Hynobius retardatus). Methods: Rana pirica tadpoles were exposed to the predator signal in close proximity to or remote from the dragonfly larvae or the salamander larvae to determine whether the tadpoles develop predator-specific morphologies and whether they utilize predator-specific signals in the induction process. We conducted predation trials to determine whether the tadpoles with induced phenotypes were more resistant to the attack in the corresponding predator environment. Results: Rana pirica tadpoles developed predator-specific morphologies in response to exposure to two different types of predator. The tadpoles discriminated between the predators that is, different signals were required to develop the specific phenotypes in the induction process. The survival rate of tadpoles of specific phenotypes was higher than that of tadpoles of mismatched or non-induced phenotypes when exposed to predation by the corresponding predators.
  • T Mori, Hiraka, I, Y Kurata, H Kawachi, O Kishida, K Nishimura
    BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 330 (4) 1138 - 1145 0006-291X 2005/05 [Not refereed][Not invited]
     
    Anuran tadpoles (Rana pirica) are induced to develop a higher tail and a bulgy body as predator-specific morphological responses when they are exposed to predatory larval salamanders. Subtractive hybridization was performed using induced tadpole body skin and normal tadpoles' body skin. A total of 196 clones showed higher expression, and 104 clones showed lower expression, when they formed bulgy bodies. In the subtraction, carboxypeptidase 13, trypsinogen, elastase 1, fibrinogen, elastase 11, triacyl-glycerol lipase, and alpha 1-antitrypsin genes showed lower expression. In contrast, RT-like protein, bullous pemphigoid antigen, phosphoserine aminotransferase, uromodulin, tetranectin, chaperonin-like protein, zinc finger protein, osteonectin, aldehyde dehydrogenase, Sec 23A protein, and ribosomal protein showed higher gene expression. Microarray analysis was also performed using this subtracted cDNA (nine replicates). Results of the microarray data essentially corresponded with those of the subtraction data, and the degree of the suppressed genes was much stronger than that of the expressed genes. Carboxypeptidase B showed the strongest suppression, and its inhibition range was from 1/100 to 3/100 compared with that of control body skin. Strong suppression was also observed with trypsinogen, elastase 1, fibrinogen, and elastase 11 as well. These results can be interpreted as increases of fibrinolysis by strong depression of both carboxypeptidase B and other genes simultaneously, resulting in the retention of blood vessels and facilitating the circulation of blood. Expression was observed in phosphoserine aminotransferase, aldehyde dehydrogenase, RT-related protein, chaperonin-like protein, tetranectin, bullous pemphigoid antigen, uromodulin, and Sec 23A protein. They were significantly (p < 0.05) increased and were at least 1.5 times greater compared with the control. From the appearance, it seems that the bulgy shaped body is highly connecting to the bullous pemphigoid (BP) antigen that causes the skin blistering disorder, and tetranectin and uromodulin may be related to the extracell matrix through myogenesis, protein secretion, and ion transport, respectively. Since the RT-related protein gene derived from retrotransposon (L1) is known to disrupt mammalian transcriptomes, retrotransposon may be involved with phenotypic plasticity for morphological defense by Rana prica against predator threat. (c) 2005 Elsevier Inc. All rights reserved.
  • O Kishida, K Nishimura
    OECOLOGIA 140 (3) 414 - 421 0029-8549 2004/08 [Refereed][Not invited]
     
    Predator induced morphological defenses are marked morphological shifts induced directly by cues associated with a predator. Generally, remote cues, i.e., chemical substances emitted from predators or injured conspecifics, are considered to be ideal signals to induce morphological change in aquatic environments rather than close cues, i.e., close chemical or tactile cues, since chemical substances that can propagate over relatively long distances and persist for a long period may allow organisms to keep safe and to deliberately change their morph. In fact, most organisms adopting an inducible morphological defense utilize remote chemical cues to detect predation risk and to produce morphological defenses. In this paper, we report a unique and functionally well designed inducible morphological defense strategy where the induction process requires close cues from a predator. The tadpoles of Rana pirica exhibited a bulgy bodied morphology when threatened with predation by larval salamanders, Hynobius retardatus, in close proximity. Predation trials and a function experiment showed that the induced bulgy morph is an adaptive defense phenotype against the gape-limited predator larval H. retardatus. Furthermore, R. pirica tadpoles use two adaptive strategies in terms of cost saving, i.e., adjustment of the extent of bulginess according to predation risk and reversibility by actual shrink of bulgy body after removing the predation threat. In general, R. pirica hatch earlier than H. retardatus. In natural ponds, during the early developmental stage R. pirica tadpoles live in close proximity to young H. retardatus larvae. As they grow, the salamanders gradually become serious predators and the predator-prey interaction becomes intimate. After a while, predation, cannibalism and metamorphosis decrease the number of salamanders in the ponds, and the predator-prey interaction weakens. Such a phenology in the predator-prey interaction allows the evolution of a close-cue detection system and adaptive cost-saving strategies. Our results highlight that the characteristics of the inducible defense depend on the intensity and specificity of the predator-prey system.
  • Kinya Nishimura, Osamu Kishida
    ECOLOGICAL RESEARCH 16 (3) 359 - 368 0912-3814 2001/09 [Refereed][Not invited]
     
    Coupling of two Lotka-Volterra type competition systems with density-dependent migration was surveyed. We assumed that species x and y are each exclusively superior in subhabitat 1 and subhabitat 2, respectively, and that population densities that exert intra-and interspecific competitive effects also impose pressures for migration of individuals from a subhabitat. If the two species are, respectively, abundant in the subhabitats in which either species is competitively superior, and the migration has a mixing effect, then, it would be intuitively expected that, as potential migration rates increase, the two species are mixed well and coexist in the whole habitat. An analysis of this competitive situation using our model under the assumption of linear diffusion predicted that, even though weak mixing maintains coexistence in the whole habitat, strong mixing collapses coexistence and leads to the exclusion of one species. The assumption that migrations occur due to self- and cross-population pressures provides different predictions: (i) weak dominance and strong mixing destabilize the coexistence state and lead to a monopolizing equilibrium of either species (bistability of monopolizing equiliblia); (ii) conspicuous weakness of the inferior species makes the mixing equilibrium stable, regardless of the potential migration rate; and (iii) tri-stability exists in between situations (i) and (ii). In the third case, the attainable state is the mixing equilibrium or either of the monopolizing equilibria, depending on the initial state. Migration mechanisms with self- and cross-population pressures tends to mediate spatial segregation and makes coexistence possible, even with strong mixing.

Books etc

  • 多種系における表現型可塑性（分担執筆） シリーズ群集生態学2 進化生物学からせまる
    京都大学学術出版会 2009

MISC

Awards & Honors

  • 2009 第13回 日本生態学会宮地賞

Research Grants & Projects

  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2022/04 -2027/03 
    Author : 北野 潤, 岸田 治, 石川 麻乃, 山崎 曜, 山道 真人
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2022/04 -2026/03 
    Author : 岸田 治
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2020/07 -2022/03 
    Author : Kishida Osamu
     
    Movement of animals is a key for deepening our understanding of ecology of animals. In this study, we explored what kind of mortality pressure operate on the individuals during their movement, and what tactics animals take against the mortality pressure. We addressed these issues by focusing migration of masu salmon juveniles by conducting individual survey using a PIT tag system. First, we found that river-descending migrants were exposed to size-dependent mortality, in which smaller individuals suffer higher mortality pressure. Second, we showed that smaller migrants exhibited higher growth rate in the pre-migration period and descend the river in later timing than larger migrants. Because the faster growth and later start of migration of smaller migrants allow them to become into larger size before migration, these life history and behavioral pattens represent tactics under size-dependent mortality in the migration.
  • Ecology of Size Dynamics
    Ministry of Education, Culture, Sports, Science and Technology：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2017/04 -2022/03 
    Author : Osamu Kishida
  • 北海道に侵入したアズマヒキガエルが水域の生物 群集に与える影響
    THE ASAHI GLASS FOUNDATION：THE ASAHI GLASS FOUNDATION RESEARCH GRANT
    Date (from‐to) : 2017/04 -2020/03 
    Author : Osamu Kishida
  • 北海道に侵入した強毒性ヒキガエルのインパクト
    MITSUI & CO., LTD.：The Mitsui & Co. Environment Fund
    Date (from‐to) : 2017/04 -2020/03 
    Author : Osamu Kishida
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2015/04 -2018/03 
    Author : SATO Takuya, HIURA Tsutomu, KISHIDA Osamu, UTSUMI Syunsuke
     
    In this research project, we examined the causes and consequences of temporal variation in subsidies in stream and riparian ecosystems. A large-scale monitoring revealed that phenological diversity of arthropods and their nematomorph parasites synergistically determined the duration and seasonal timing of the riparian subsidies into streams. A field experiment then revealed that the pulsed subsidy allowed salmonid fish grow more evenly among individuals, which had different cascading effects on benthic invertebrates and leaf breakdown rate compared with the prolonged subsidy. In another experiment, fish exhibited a higher numerical response to the early subsidy, but not to the late subsidy, with the timing-dependent life history adoptions and its diversity. By using these empirical results, two modeling approaches highlight underappreciated roles of phenological variation in the assemblages of across-habitat consumer and resource movements in driving community and disease dynamics.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2014/04 -2016/03 
    Author : KISHIDA Osamu, KOBAYASHI Makoto
     
    Aim of this study is to suggest a possibility of dissolved-amino-acid-usability for aquatic animals, by using larvae of Hynobius retardatus salamanders. As a result of multiple experiments, we show that the salamander larvae took in nitrogen from dissolved amino acids, and promoted their growth when they were kept in environmental water added to amino acids. Until now, aquatic prokaryotes such as bacteria are known to absorb dissolved amino acids directly from environmental water as an energy source for population growth. However, it has been assumed that aquatic vertebrates do not utilize them. The present finding may require the conventional view about energy flow in aquatic systems to be revised.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2011/04 -2016/03 
    Author : Nishimura Kenya, MIURA Toru, KISHIDA Osamu, MICHIMAE Hirofumi, KITANO Jun
     
    The Hokkaido salamander (Hynobius retardatus) is an endemic species inhabiting in Hokkaido Japan. Larvae of the Hokkaido salamander exhibit phenotypic plasticity that associate with defense against predators, offense to prey and conspecific larvae. The larval phenotypic plasticity is an eligible phenomenon for the integrative study of evolutionary ecology and molecular developmental biology. In this project, I tried to investigate, (1) morphological changes associated with the phenotypic plasticity by geometric morphometric analysis, (2) the genomic information about the morphological changes with the phenotypic plasticity by a RNAseq analysis, and (3) variations of morphology and morphological changes (developmental reaction norm) and microsatellite polymorphism among five local populations in the whole distribution area of the endemic species.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2011 -2013 
    Author : MICHIMAE Hirofumi, KISHIDA Osamu
     
    In nature, organisms constantly face multiple environments, and the expression and magnitude of the costs of plastic traits is occasionally context-dependent; therefore, the costs need to be analyzed across multiple environments. We determined the benefits and costs of two plastic responses (predator- and prey-induced morphologies) of larvae of the salamander Hynobius retardatus on larval survival, metamorphic timing, and body size at metamorphosis in three different environments by using frog tadpoles, predatory dragonfly larvae, or no inducer (conspecific larvae only). The benefits of plastic responses were detected in the inducing environments, but the costs were greater or more easily detected in crossover environments, such as those containing tadpoles or dragonfly larvae. The trade-offs appeared in combinations in the crossover environments, and thus were context-dependent.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2012 -2012 
    Author : KISHIDA Osamu
     
    Individuals are not uniform even within a species. Using a forest pond community as a model system, I experimentally explored ecological consequences of intra-population trait variation in a predator and prey species. I found that Intra-population trait variation of predator (Hynobius retardatus, salamander larvae) and prey (Rana pirica, tadpoles) species strongly dictate structure of inter-specific interactions through occurrence of intra-specific interaction such as cannibalism and apparent competition. Importantly, such effects translate into impacts on demography and evolution of community members and material flow within and between ecosystems. This study generally highlights that incorporating trait variation within a species into community ecology is imperative to deepen our understanding of dynamics and function of ecological community in nature.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2010 -2012 
    Author : SAITOH TAKASHI, KISHIDA Osamu, ISHIBASHI Yasuyuki
     
    Since most populations long sustain themselves in their mutual interaction, the knowledge about the population structure is essential to understand a mechanism of their sustainability. In this study I investigated the structure of a rodent population for 4 years taking their dynamics (genetic drift) and dispersal (gene flow) into consideration. The main results are as follows: (1) A scale of gene flows differed between sexes. Females' scale (500 m) was smaller than males' (2000 m); (2) The spatial structure differed between mtDNA-based and microsatellite DNA-based structure. A microsatellite DNA-based population included several mtDNA-based populations; (3) Effects of population dynamics was significant in females. Effects of genetic drift dominated over those of gene flow in a low density year.
  • Japan Society for the Promotion of Science：Grants-in-Aid for Scientific Research
    Date (from‐to) : 2010 -2011 
    Author : KISHIDA Osamu
     
    Ecological consequences of inducible offense and defense are explored using predator Hynobius retardatus salamander larvae and prey Rana pirica frog tadpoles. We experimentally demonstrated that the antagonistic inducible responses of the predator and prey impact on population dynamics of prey tadpoles and life history of both species. We also found that the modification of the population level effects affect abundance of invertebrate community and ecosystem function
  • 文部科学省：科学研究費補助金(若手研究(スタートアップ), 研究活動スタート支援)
    Date (from‐to) : 2009 -2010 
    Author : 岸田 治
     
    変化する生物群集のなかで生物個体は形質をどのように変えるのか?その結果として個体群や群集レベルでどのような帰結がもたらされるのか?個体の応答性と高次の生態学的要素との相互関係の理解は、表現型可塑性研究の新しいムーブメントである。平成21年度は、1.この未開の領域において優先的に取り組まれるべき課題を明らかにするため、捕食者-被食者系の表現型可塑性に関する最近の研究の論点と成果をまとめた。その結果、(1)3種以上の相互作用系での個体の形質変化、(2)複数の誘導形質間の発現・機能上の関係性、(3)捕食者の可塑性による相互作用強度の変更、(4)捕食者と被食者の対抗性とその生態学的な影響、等のトピックについての理解が不足していることがわかった。そこでこれらについて理論的・実証的に研究する方法を提案した(以上は、総説論文として、Population Ecology誌に公表した)。2.次にトピック(4)に関する理論的研究を行った。捕食者と被食者の対抗的な可塑性の進化動態と個体群動態を数学的にモデル化し解析したところ、被食者が効果的な防御をもつときに捕食者と被食者の対抗的な可塑性が共進化しやすく、2種の個体群動態が安定的に持続することが分かった。3.最後に、個体の可塑性の群集生態学的影響を定量的に評価するためのモデル実験系を確立した。報告者はこれまでに可塑性研究の有効なモデル系として、エゾ...
  • Evolutionary Ecology of Phenotypic Plasticity in Amphibian Larvae.

Educational Activities

Teaching Experience

  • Advanced Course in Forest Sphere Science III (Conservation Biology)
    開講年度 : 2021
    課程区分 : 修士課程
    開講学部 : 環境科学院
    キーワード : 動物生態学，保全，野外調査，研究発表 Animal Ecology, Conservation, Field Investigation, Presentation
  • Inter-Graduate School Classes(General Subject):Natural and Applied Sciences
    開講年度 : 2021
    課程区分 : 修士課程
    開講学部 : 大学院共通科目
    キーワード : 生態学、北方生態系、北海道、植物、動物、昆虫、魚類、森林、山岳、ツンドラ、沿岸、河川、湿原、相互作用、外来種、野生作物、気候変動 ecology, northern ecosystem, Hokkaido, plants, animals, insects, fishes, forest, mountain, tundra, seacoast, river, wetland, interaction, invasive species, field crop, climate change
  • Fundamental Course in Biodiversity of Northern Ecosystems
    開講年度 : 2021
    課程区分 : 修士課程
    開講学部 : 環境科学院
    キーワード : 生態学、北方生態系、北海道、植物、動物、昆虫、魚類、森林、山岳、ツンドラ、沿岸、河川、湿原、相互作用、外来種、野生作物、気候変動 ecology, northern ecosystem, Hokkaido, plants, animals, insects, fishes, forest, mountain, tundra, seacoast, river, wetland, interaction, invasive species, field crop, climate change
  • Advanced Course in Animal Ecology II
    開講年度 : 2021
    課程区分 : 修士課程
    開講学部 : 環境科学院
    キーワード : 動物、個体群、群集、行動、保全、進化、種間相互作用 Animal, population, community, behavior, conservation, evolution, species interaction
  • Practical Field Work on Wildlife Conservation
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 農学部
    キーワード : 野生動物調査，動物生態学，捕獲法，マーキング，群集解析，哺乳類，鳥類，魚類，昆虫類
  • Wildlife Management
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 農学部
    キーワード : 保全, 群集, 個体群, 生物多様性, 進化，外来種種
  • Forest Influence
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 農学部
    キーワード : 森林、環境保全機能、生物多様性保全、野生生物保全、土地利用、流域保全、森林利用
  • Seminar on Forest Influence
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 農学部
    キーワード : 森林の種類と分布、森林空間、環境保全機能、森林保全、資料作成方法、発表方法、ディスカッション
  • Freshman Seminar
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 全学教育
    キーワード : 生態学、観察実験、進化、食う―食われる関係、温暖化、リモートセンシング、樹木、両生類、昆虫、土壌、グループワーク
  • Freshman Seminar
    開講年度 : 2021
    課程区分 : 学士課程
    開講学部 : 全学教育
    キーワード : 洞爺湖の環境、有珠山噴火、有珠山植生回復、海藻の生態、森林の生態

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