Yoshino Ando

Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web

Plants have diverse ways of responding to damage by herbivores, such as changes in allelochemistry, physiology, morphology, growth, and phenology. These responses form the mechanistic basis for trait-mediated indirect interactions (TMIIs) between organisms on the plants. There is a growing appreciation that such TMIIs form complex networks (i.e., indirect interaction webs) in terrestrial plant-associated arthropod communities. Almost all previous studies have had the same framework: examining trait-mediated indirect effects within a single interactive unit consisting of one initiator of herbivore, a host plant as a mediator, and one receiver [trait-mediated indirect interaction unit (TMIU)]. However, this framework is too simple to understand the dynamics of the indirect interaction web. Recent studies suggest that there is a wide variety of interactions among TMIUs within a community, which may largely affect the outcomes of indirect effects in each unit. Here, we review recent advance in studies of trait-mediated indirect effects in plant-associated arthropod communities and explore the mechanisms of linkages among TMIUs. Then, we argue the importance of examining linkages among TMIUs as a new framework for future studies on the indirect interaction web. Finally, we propose the hypothesis that linkages among TMIUs contribute to the maintenance of biodiversity.

Plant genotypic diversity increases population size of a herbivorous insect

It is critical to incorporate the process of population dynamics into community genetics studies to identify the mechanisms of the linkage between host plant genetics and associated communities. We studied the effects of plant genotypic diversity of tall goldenrod Solidago altissima on the population dynamics of the aphid Uroleucon nigrotuberculatum. We found genotypic variation in plant resistance to the aphid in our experiments. To determine the impact of plant genotypic diversity on aphid population dynamics, we compared aphid densities under conditions of three treatments: single-genotype plots, mixed-genotype plots and mixed-genotype-with-cages plots. In the latter treatment plants were individually caged to prevent natural enemy attack and aphid movement among plants. The synergistic effects of genotypes on population size were demonstrated by the greater aphid population size in the mixed-genotype treatment than expected from additive effects alone. Two non-exclusive hypotheses are proposed to explain this pattern. First, there is a source–sink relationship among plant genotypes: aphids move from plant genotypes where their reproduction is high to genotypes where their reproduction is low. Second, natural enemy mortality is reduced in mixed plots in a matrix of diverse plant genotypes.

Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant.

Much attention has been paid to ecology and evolution of damage-induced plant responses. Recently, it has been emphasized that phenotypic plasticity, such as induced plant responses, has the potential to lead to evolutionary changes of interacting partners. Here, we report that induced plant regrowth promotes a locally adaptive feeding preference of a leaf beetle, Plagiodera versicolora. We found that there was among-population variation in the strength of the feeding preference of the leaf beetle for leaf-age types of conspecific host plants. The strength of the preference was positively correlated to leaf production of host plants across populations, and the intensity of induced regrowth was likely to have been responsible for geographic variation in new leaf production. Within one population, we detected a significant additive genetic variance and heritability in the preference for consuming new vs. old leaves. Moreover, the strength of preference was significantly related to egg production depending on the leaf-age types. Thus, allopatric populations can evolutionarily develop different adaptive preference, according to locally distinct patterns of induced host regrowth.

Herbivore community promotes trait evolution in a leaf beetle via induced plant response

Several recent studies have emphasised that community composition alters species trait evolution. Here, we demonstrate that differences in composition of local herbivore communities lead to divergent trait evolution of the leaf beetle Plagiodera versicolora through plant-mediated indirect interactions. Our field surveys, genetic analyses and community-manipulation experiments show that herbivore community composition determines the degree of herbivore-induced regrowth of willows (Salicaceae), which in turn, promotes the divergent evolution of feeding preference in the leaf beetle from exclusive preference for new leaves to a lack of preference among leaf-age types. Regrowth intensity depends both on the differential response of willows to different herbivore species and the integration of those herbivore species in the community. Because herbivore-induced regrowth involves phenological changes in new leaf production, leaf beetle populations develop divergent feeding preferences according to local regrowth intensity. Therefore, herbivore community composition shapes the selection regime for leaf beetle evolution through trait-mediated indirect interactions.

Ant- and plant-mediated indirect effects induced by aphid colonization on herbivorous insects on tall goldenrod

We studied the indirect effects of an aphid Uroleucon nigrotuberculatum on density and performance of herbivorous insects through tending ants and modification of plant traits on a tall goldenrod Solidago altissima in Japan. To examine ant-mediated indirect effects of the aphid on the leafhopper and geometrid moth caterpillars, we conducted an experiment in which we manipulated aphid densities. The aphid decreased the density of these herbivorous insects through ant-mediated indirect effects, because honeydew scattered by the aphid-attracted ants that then removed them. To examine plant-mediated indirect effects of the aphid on two temporally separated insects, a scale insect and a grasshopper, we compared the density and performance of these herbivorous insects on aphid-inoculated plants and aphid-free plants. Aphid-induced plant modifications had different effects on the scale insect and grasshopper. The aphid indirectly decreased the density and survivorship of the scale insect. On the other hand, the number of grasshoppers increased as a result of the increased number of leaves and the increased nitrogen content induced by prior aphid feeding. However, aphid infestation did not affect the survival of the grasshopper. Thus, the aphid has large indirect effects on co-occurring herbivorous insects through the removal behavior of tending ants and on temporally separated herbivorous insects through changes in quality and quantity of the tall goldenrod.

Community-wide impact of an exotic aphid on introduced tall goldenrod.

1. The aphid Uroleucon nigrotuberculatum Olive, which is specialised to the tall goldenrod, Solidago altissima L., in its native range, has become a dominant species on the introduced tall goldenrod in Japan. How this exotic aphid influenced arthropod communities on the introduced tall goldenrod in aphid‐present (spring) and aphid‐absent (autumn) seasons was examined, using an aphid removal experiment.

Community structure of insect herbivores on introduced and native Solidago plants in Japan

We compared community composition, density, and species richness of herbivorous insects on the introduced plant Solidago altissima L. (Asteraceae) and the related native species Solidago virgaurea L. in Japan. We found large differences in community composition on the two Solidago species. Five hemipteran sap feeders were found only on S. altissima. Two of them, the aphid Uroleucon nigrotuberculatum Olive (Hemiptera: Aphididae) and the scale insect Parasaissetia nigra Nietner (Hemiptera: Coccidae), were exotic species, accounting for 62% of the total individuals on S. altissima. These exotic sap feeders mostly determined the difference of community composition on the two plant species. In contrast, the herbivore community on S. virgaurea consisted predominately of five native insects: two lepidopteran leaf chewers and three dipteran leaf miners. Overall species richness did not differ between the plants because the increased species richness of sap feeders was offset by the decreased richness of leaf chewers and leaf miners on S. altissima. The overall density of herbivorous insects was higher on S. altissima than on S. virgaurea, because of the high density of the two exotic sap feeding species on S. altissima. We discuss the importance of analyzing community composition in terms of feeding guilds of insect herbivores for understanding how communities of insect herbivores are organized on introduced plants in novel habitats.

Bridges and barriers to host shifts resulting from host plant genotypic variation

Abstract Host-associated differentiation is hypothesized to be one of the primary means by which new species of herbivorous insects evolve. Divergent selection for host plant use following a host shift is a critical assumption of host-associated differentiation. Host shifts are more likely to occur between closely related host species, and the probability of a host shift and of the evolution of reproductive isolation depends on the genetic variation within both the host plant population and the herbivorous insect. We have been studying the evolution of reproductive isolation in populations of Eurosta solidaginis that form galls on Solidago altissima altissima and Solidago altissima gilvocanescens. Each of the Eurosta populations is a host race that is partially but incompletely isolated from the other host races by its adaptation to its host plants. The Solidago sp. populations show high intraspecific variation within and among populations in their resistance to attack by the host races which are adapted to them. There is also evidence that they vary in their susceptibility to host races adapted to other Solidago species. We examine the hypothesis that the intraspecific Solidago variation determines the degree of gene flow among Eurosta populations and that this can create barriers or bridges to gene flow and therefore determine the course of speciation in these insects. The intraspecific host plant variation can influence the interactions with herbivores when it is an invasive species. The restricted range of genetic variation introduced into a new region may be a good or poor match with populations of herbivores that are also introduced into the new area.

Metagenomic Approach Yields Insights into Fungal Diversity and Functioning

Recent advances in molecular biological methods have drastically changed our understanding of the diversity, phylogeny, ecology, and evolution of fungi. The purpose of this chapter is to address recent progress in our knowledge about the biodiversity of fungi, with emphasis on the potential impact of pyrosequencing to estimate fungal diversity in environmental samples. Progress in DNA sequence-based techniques notably enables us not only to overcome potential flaws of traditional mycological techniques but also to evaluate fungal richness more efficiently and reliably. Especially, the development of next-generation sequencing technologies has revolutionized large-scale sequencing of environmental fungal DNA. A number of papers have been published regarding metagenomic analysis of fungal diversity in environmental samples, using Roche 454 pyrosequencing since 2009. The number of publications on fungal metagenomics will be accelerated, but there are potential methodological difficulties that have not been solved yet. DNA barcoding with universal genetic markers and high-quality sequence databases becomes more important as reliable taxonomic affiliations of numerous MOTUs are necessitated. Further studies are needed to test the applicability of pyrosequencing to such hot spots of fungal diversity as tropical forests and to explore functional aspects of fungal populations.

Indirect interaction webs on tall goldenrod: community consequences of herbivore-induced phenotypes and genetic variation of plants

Abstract Tall goldenrod, Solidago altissima, was introduced from North America 100 years ago, and it has become widely distributed all over Japan. We have been investigating plant-based indirect interaction webs on the tall goldenrod in Japan and the US. We found that arthropod communities on Japanese goldenrods are organized via plant- and ant-mediated indirect effects caused by the dominant aphid, Uroleucon nigrotuberculatum, which came from the US in the early 1990s. The aphid also generated bottom-up cascading effects on temporally separated communities. Our results highlight the importance of herbivore-induced plant phenotypes in determining the structure of indirect interaction webs. We review our ongoing research that focuses on the effect of plant genotypic variation on the formation of indirect interaction webs. Our findings of the genotypic effects on aphid population dynamics and herbivore community composition provide a more complete understanding of the community consequences of plant genotypic diversity, as well as herbivore-induced plant phenotypes.