Article

Structure of the Encounter between Goldenrod (Solidago Altissima) and Its Diverse Insect Fauna

Wiley
Ecology
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Abstract

Examined population responses of 17 insect species to genotypic variation exhibited by clones of Solidago altissima. Cluster analysis on the genetic correlations between the insects' responses produced four groups, termed "herbivore suites', that are attracted and repelled by similar plant genotypes (and their underlying sets of traits). There was no obvious correspondence of an insect's phylogenetic affinity, host range, or feeding style with its membership in a particular suite. The genetic variability of the plant population will be reflected in the diversity and composition of the insect community. Selection caused by one herbivore species can result in increased resistances to other rarer species whose responses are correlated with those of the damaging species. Selection by suites of herbivores may be more intense and less variable than selection by individual insect species, especially when many species are rare. -from Authors

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... introduCtion Genetic variation within host-plant species is a key factor governing its associated arthropods (Fritz and Price 1988, Maddox and Root 1990, Johnson 2008. Studies have now shown that the effects of host-plant genetic variation can extend beyond herbivores (Fritz and Price 1988, Maddox and Root 1990, Barbour et al. 2015 to determine predator abundances (Bailey et al. 2006, Johnson 2008) and the structure of trophic interactions (Barbour et al. 2016). ...
... introduCtion Genetic variation within host-plant species is a key factor governing its associated arthropods (Fritz and Price 1988, Maddox and Root 1990, Johnson 2008. Studies have now shown that the effects of host-plant genetic variation can extend beyond herbivores (Fritz and Price 1988, Maddox and Root 1990, Barbour et al. 2015 to determine predator abundances (Bailey et al. 2006, Johnson 2008) and the structure of trophic interactions (Barbour et al. 2016). The few studies that have examined potential mechanisms underlying the communities of higher trophic levels on host-plants suggest that genetic variation in plant traits indirectly affects predators primarily through variation in herbivore abundances and traits (Bailey et al. 2006, Johnson 2008, Mooney and Agrawal 2008, Barbour et al. 2016). ...
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Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities.
... introduCtion Genetic variation within host-plant species is a key factor governing its associated arthropods (Fritz and Price 1988, Maddox and Root 1990, Johnson 2008. Studies have now shown that the effects of host-plant genetic variation can extend beyond herbivores (Fritz and Price 1988, Maddox and Root 1990, Barbour et al. 2015 to determine predator abundances (Bailey et al. 2006, Johnson 2008) and the structure of trophic interactions (Barbour et al. 2016). ...
... introduCtion Genetic variation within host-plant species is a key factor governing its associated arthropods (Fritz and Price 1988, Maddox and Root 1990, Johnson 2008. Studies have now shown that the effects of host-plant genetic variation can extend beyond herbivores (Fritz and Price 1988, Maddox and Root 1990, Barbour et al. 2015 to determine predator abundances (Bailey et al. 2006, Johnson 2008) and the structure of trophic interactions (Barbour et al. 2016). The few studies that have examined potential mechanisms underlying the communities of higher trophic levels on host-plants suggest that genetic variation in plant traits indirectly affects predators primarily through variation in herbivore abundances and traits (Bailey et al. 2006, Johnson 2008, Mooney and Agrawal 2008, Barbour et al. 2016). ...
Article
Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities. This article is protected by copyright. All rights reserved.
... The asymmetric nature of interactions between individual host plant species and multiple herbivores suggests that the evolution of defense is most commonly diffuse in nature (Maddox & Root, 1990;Simms, 1990;Strauss et al., 2005;Wise & Rausher, 2013). In such scenarios, the direction and magnitude of selection by a given herbivore will depend on the selection by other attackers as well. ...
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A major predicted constraint on the evolution of anti-herbivore defense in plants is the non-independent expression of traits mediating resistance. Since herbivore attack can be highly variable across plant tissues, we hypothesized that correlations in toxin expression within and between plant tissues may limit population differentiation and, thus, plant adaptation. Using full-sib families from two nearby (<1 km) common milkweed (Asclepias syriaca) populations, we investigated genetic correlations among 28 distinct cardenolide toxins within and between roots, leaves and seeds, and examined signatures of tissue-specific divergent selection between populations by QST-FST comparisons. The prevalence, direction and strength of genetic correlations among cardenolides were tissue-specific, and concentrations of individual cardenolides were moderately correlated between tissues; nonetheless, the direction and strength of correlations were population-specific. Population divergence in the cardenolide chemistry was stronger in roots than in leaves and seeds. Divergent selection on individual cardenolides was tissue- and toxin-specific, except for a single highly toxic cardenolide (labriformin), that showed divergent selection across all plant tissues. Heterogeneous evolution of cardenolides within and between tissues across populations appears possible due to their highly independent expression. This independence may be common in nature, especially in specialized interactions in which distinct herbivores feed on different plant tissues.
... Why was there no direct effect of S. canadensis on arthropod richness and abundance when so many other studies (Abrahamson & Weis, 1997;Carson & Root, 2000;Crutsinger et al., 2009;Crutsinger, Reynolds, et al., 2008; T A B L E 1 Results from linear regressions predicting the effect of Solidago canadensis biomass, subdominant plant biomass, and subdominant plant species richness on arthropod community trophic mean and herbivore, detritivore, omnivore, and predator abundance. Dudek et al., 2016;Fenesi, V ag asi, et al., 2015;Maddox & Root, 1990) have shown that Solidago species clearly do affect arthropod richness and abundance? The arthropod fauna associated with many Solidago species is well documented and studied. ...
Article
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Dominant plant species are locally abundant and have large impacts on ecological communities via a variety of mechanisms. However, few studies have evaluated the influence of a dominant plant species both within and among trophic levels and on key ecosystem functions such as productivity. In this study, we evaluated the effect of the dominant plant species Solidago canadensis on plant and arthropod communities in an old‐field ecosystem in southeastern Michigan. We found that S. canadensis negatively correlated with the richness and combined biomass of all other plant species in the community, likely by reducing light availability. In turn, less biomass of all other plant species led to lower arthropod abundance. Specifically, detritivore and predator arthropod abundance was lower with less biomass of all plant species excluding S. canadensis, but herbivore and omnivore abundance was unaffected. Our results highlight the significant role of dominant plants in determining plant diversity and ecosystem function, and further suggest that the effect of a dominant plant species on a community is observed at higher trophic levels.
... This area at the canopy level. Other important plant genera in the hydric forest, such as Geum, Solidago, and Rubus, have also been previously shown to attract large insect assemblages (Maddux and Root 1990, Johnson et al. 2003, Wignall et al. 2020. The lack of pitfall insect association with any specific plant genus, despite the distinctness of hardwood and hydric assemblages, suggested the general differences between the two forests reflected in ground-dwelling insects that are less dependent on specific plant species (McCravy and Lundgren 2011). ...
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The effects of plants on insects are not completely clear due to potential covariation of weather or location affecting both assemblages. To address this question, plant and insect assemblages were described during summer 2019 and 2020 in two different forest habitats of northern Lower Michigan. The first habitat was a hardwood forest typical of secondary succession in the region. The second was a hydric forest located ~20 m from the hardwood forest which developed after lake sediment was deposited into a 10-ha area in the early 2000s. Reflecting this sediment deposition, soil of the hydric forest had higher water content and organic matter, and was dominated by the plant genera Solidago (Asterales: Asteraceae), Rubus (Rosales: Rosaceae), and Salix (Malpighiales: Salicaceae). In contrast, the hardwood forest had greater inorganic sediment and was dominated by Pteridium (Polypodiales: Dennstaedtiaceae), Carex (Poales: Cyperaceae), and Acer. Nearly 140,000 insect specimens were sampled using pitfall trapping, sweep netting, flight intercept trapping, ultraviolet light trapping, and yellow and blue pan trapping. The first three methods each sampled a unique insect assemblage, whereas the last three overlapped in taxa sampled. Insect assemblages of the two forests were distinct from each other using any of the six methods, with abundance of Pteridium and Salix (Sapindales: Sapindaceae) generally associating with changes in insect composition. A total of 41 insect taxa indicated the hydric forest and 14 indicated the hardwood forest. Insect richness increased with that of plants. These results demonstrate that differences in soil composition and plant assemblages associate with differences in forest insect assemblages, even of forests in very close proximity.
... Host preferences can be partially determined from the strength of the effect of top predators and parasitoids on the lower trophic levels, which varies with their abundance and efficiency [2,3], but mostly from host-related variables [4]. Plant variables such as the number of young leaves, leaf production, palatability, water content, plant height, nitrogen content, phenotypic variability, and secondary compounds determine the nutritional and mechanical properties of plants as hosts for herbivores [5][6][7][8][9]. The aforementioned differences in plant traits are local and can be linked with smallscale genetic differentiations among plant populations [10], which alongside the physical conditions of different habitats and the competition or presence of (mycorrhizal) fungi can be caused by the herbivores themselves [11][12][13][14]. ...
Article
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Intrataxonomic differences in terms of angiosperm suitability for herbivorous insects stem from variables such as plant structure, palatability, and chemistry. It has not yet been elucidated whether these differences also occur in terms of the bryophyte's suitability to bryophages. Hypnum cupressiforme Hedw. is a morphologically variable moss species frequently inhabited or fed by insects. In this investigation, we offered five morphotypes of H. cupressiforme to two bryophagous species of Byrrhidae (Coleoptera) to reveal whether the intrataxonomic variability affects beetles' preferences. The morphotypes were offered with preserved and removed spatial structures. There were no significant differences in morphotype preferences when spatial structures were preserved, although during the daytime, the beetles moved from the flat morphotype to the usual and turgid morphotypes. The beetles preferred the turgid morphotype when the spatial structures were removed. The results suggest that the spatial structure variations in the H. cupressiforme complex are accompanied by different chemical, physiological, or microscopic morphological profiles that are recognized by the bryophagous insects. Phylogenetic and epigenetic analyses can reveal multiple differences within the H. cupressiforme complex. Their interconnection with information about the preferences of bryophagous insects can help us to elucidate which of these differences are ecologically relevant.
... On the other hand, different consumers may impose selection on different traits, favoring trait integration and increasing genetic constraints. Examples of this include strong genetic covariances in plant 312 resistance to different insect herbivores (Maddox and Root, 1990;Wise, 2007;Wise and Rausher, 2013), although there are also examples where these covariances are weak (Roche and Fritz, 1997;Barbour et al., 2015), or vary from year-to-year (Johnson and Agrawal, 2007). We suggest that 315 gaining predictive insight to the evolutionary consequences of food-web disassembly requires an understanding of the mechanisms governing the assembly of trophic interactions. ...
Article
Full-text available
Global change is simplifying the structure of ecological networks; however, we are currently in a poor position to predict how these simplified communities will affect the evolutionary potential of remaining populations. Theory on adaptive landscapes provides a framework for predicting how selection constrains phenotypic evolution, but often treats the community context of evolving populations as a “black box”. Here, we integrate ecological networks and adaptive landscapes to examine how changes in food-web complexity shape evolutionary constraints. We conducted a field experiment that manipulated the diversity of insect parasitoids (food-web complexity) that were able to impose selection on an insect herbivore. We then measured herbivore survival as a function of three key phenotypic traits. We found that more traits were under selection in simpler vs. more complex food webs. The adaptive landscape was more neutral in complex food webs because different parasitoid species impose different selection pressures, minimizing relative fitness differences among phenotypes. Our results suggest that phenotypic evolution becomes more constrained in simplified food webs. This indicates that the simplification of ecological communities may constrain the adaptive potential of remaining populations to future environmental change. “What escapes the eye, however, is a much more insidious kind of extinction: the extinction of ecological interactions.” Janzen (1974)
... Introduction A major long-established goal in community ecology and evolutionary biology is to understand how interspecific interactions influence population density, distribution, phenotypes, and genotypes [1], crucial to the selection and evolution of life-history traits. During the few last decades, the study of interspecific interactions has experienced an outstanding progress [2] such as, for example, moving from a traditional pair-wise perspective [3][4][5][6] to a more realistic and complex multispecific approach, where multiple species interact with each other [2,7,8]. However, most of these studies have focused on a single type of interaction at a time, usually studying either mutualistic or antagonistic interactions among species of particular taxonomic groups [9]. ...
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The study of plant-frugivore interactions is essential to understand the ecology and evolution of many plant communities. However, very little is known about how interactions among fru-givores indirectly affect plant reproductive success. In this study, we examined direct interactions among vertebrate frugivores sharing the same fruit resources. Then, we inferred how the revealed direct interspecific interactions could lead to indirect (positive or negative) effects on reproductive success of fleshy fruited plants. To do so, we developed a new analytical approach that combines camera trap data (spatial location, visitor species, date and time, activity) and tailored null models that allowed us to infer spatial-temporal interactions (attraction, avoidance or indifference) between pairs of frugivore species. To illustrate our approach, we chose to study the system composed by the Mediterranean dwarf palm, Cha-maerops humilis, the Iberian pear tree, Pyrus bourgaeana, and their shared functionally diverse assemblages of vertebrate frugivores in a Mediterranean area of SW Spain. We first assessed the extent to which different pairs of frugivore species tend to visit the same or different fruiting individual plants. Then, for pairs of species that used the same individual plants, we evaluated their spatial-temporal relationship. Our first step showed, for instance, that some prey frugivore species (e.g. lagomorphs) tend to avoid those C. humilis individuals that were most visited by their predators (e.g. red foxes). Also, the second step revealed temporal attraction between large wild and domestic frugivore ungulates (e.g. red deer, cows) and medium-sized frugivores (e.g. red foxes) suggesting that large mammals could facilitate the C. humilis and P. bourgaeana exploitation to other smaller frugivores by making fruits more easily accessible. Finally, our results allowed us to identify direct interaction pathways , that revealed how the mutualistic and antagonistic relations between animal associates derived into indirect effects on both plants seed dispersal success. For instance, we found that large-sized seed predators (e.g. ungulates) had a direct positive effect on the likelihood of visits by legitimate seed dispersers (e.g. red foxes) to both fleshy fruited plants. Then, seed predators showed an indirect positive effect on the plants' reproductive success.
... On the other hand, different consumers may impose selection on different traits; therefore, a more diverse consumer community may favor a particular combination of traits and increase selective constraints. Examples of this include strong genetic covariances in plant resistance to different insect herbivores (Maddox and Root 1990;Wise 2007;Wise and Rausher 2013), although there are also examples where these covariances are weak (Roche and Fritz 1997;Barbour et al. 2015), or vary from year to year (Johnson and Agrawal 2007). We suggest that gaining predictive insight to the evolutionary consequences of food-web disassembly requires an understanding of the mechanisms governing the assembly of trophic interactions (Bascompte and Stouffer 2009). ...
Article
Full-text available
The loss of biodiversity is altering the structure of ecological networks; however, we are currently in a poor position to predict how these altered communities will affect the evolution of remaining populations. Theory on fitness landscapes provides a framework for predicting how selection alters the evolutionary trajectory and adaptive potential of populations, but often treats the network of interacting populations as a “black box.” Here, we integrate ecological networks and fitness landscapes to examine how changes in food‐web structure shape phenotypic evolution. We conducted a field experiment that removed a guild of larval parasitoids that imposed direct and indirect selection pressures on an insect herbivore. We then measured herbivore survival as a function of three key phenotypic traits to estimate directional, quadratic, and correlational selection gradients in each treatment. We used these selection gradients to characterize the slope and curvature of the fitness landscape to understand the direct and indirect effects of consumer loss on phenotypic evolution. We found that the number of traits under directional selection increased with the removal of larval parasitoids, indicating evolution was more constrained toward a specific combination of traits. Similarly, we found that the removal of larval parasitoids altered the curvature of the fitness landscape in such a way that tended to decrease the evolvability of the traits we measured in the next generation. Our results suggest that the loss of trophic interactions can impose greater constraints on phenotypic evolution. This indicates that the simplification of ecological communities may constrain the adaptive potential of remaining populations to future environmental change.
... We counted the number of total leaves and the number of leaves damaged by chewing, mining, galling and sucking herbivores. The herbivore fauna associated with S. altissima in the study area is very diverse [47], but the main herbivores causing the quantified damage were T. virgata (chewing), Microrhopala virgata (mining), Asteromyia carbonifera (leaf galls), Corythucha marmorata (sucking). We also collected leaf samples for genetic analyses from the same plants (one leaf from each genotype in silica) after damage assessment. ...
Article
Plant volatile organic compounds (VOCs) are majorvehicles of information transfer between organismsand mediate many ecological interactions [1–3].Altering VOC emission in response to herbivoredamage has been hypothesized to be adaptive, asit can deter subsequent herbivores [4], attract natu-ral enemies of herbivores [5], or transmit informationabout attacks between distant parts of the sameplant [6–9]. Neighboring plants may also respondto these VOC cues by priming their own defensesagainst oncoming herbivory, thereby reducingfuture damage [10–12]. However, under which con-ditions such information sharing provides fitnessbenefits to emitter plants, and, therefore, whetherselection by herbivores affects the evolution ofsuch VOC signaling, is still unclear [13]. Here, wetest the predictions of two alternative hypotheses,the kin selection and mutual benefits hypotheses[14], to uncover the selective environment that mayfavor information sharing in plants. Measuring theresponse to natural selection inSolidago altissima,we found strong effects of herbivory on the wayplants communicated with neighbors. Plants frompopulations that experienced selection by insectherbivory induced resistance in all neighboringconspecifics by airborne cues, whereas thosefrom populations experiencing herbivore exclusioninduced resistance only in neighbors of the samegenotype. Furthermore, the information-sharingplants converged on a common, airborne VOCsignal upon damage. We demonstrate that herbivorycan drive the evolution of plant-plant communica-tion via induction of airborne cues and suggestplants as a model system for understanding infor-mation sharing and communication among organ-isms in general.
... We counted the number of total leaves and the number of leaves damaged by chewing, mining, galling and sucking herbivores. The herbivore fauna associated with S. altissima in the study area is very diverse [47], but the main herbivores causing the quantified damage were T. virgata (chewing), Microrhopala virgata (mining), Asteromyia carbonifera (leaf galls), Corythucha marmorata (sucking). We also collected leaf samples for genetic analyses from the same plants (one leaf from each genotype in silica) after damage assessment. ...
Article
Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1–3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6–9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10–12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage.We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.
... Goldenrods (Solidago and Euthamia species) are common herbs throughout the eastern United States, which have been studied extensively due to their economic importance as ornamentals, weeds, or sources of pollinators and biological control agents. Hosting a great diversity of herbivorous insects from different feeding guilds (Gagné 1968, McEvoy 1988Maddox & Root 1990;Root & Cappuccino 1992;Fontes et al. 1994), goldenrods have also served as model systems for numerous studies that focused on evolutionary and ecological aspects of speciation, resistance, and tritrophic interactions (e.g., Abrahamson & Weis 1997;Heard et al. 2006;Stireman et al. 2005Stireman et al. , 2006Wise & Abrahamson 2008, Crutsinger et al. 2009). ...
Article
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Goldenrods (Solidago and Euthamia species) are common herbs in the eastern United States that support a large and diverse community of highly specific gall-inducing insects. The majority of these insects are gall midges, of which 16 described species are bud, leaf, stem, rhizome, or flower-head gallers belonging to the large genus Rhopalomyia Rübsaamen. The present work is a taxonomic revision of the goldenrod-associated Rhopalomyia species, which includes a key to the identification of species based on their galls and host plants and descriptions of diagnostic characters for all species. Rhopalomyia lanceolata Felt is designated as a new synonym for R. lobata Felt, and R. albipennis Felt and R. carolina Felt are designated as new synonyms for R. solidaginis Loew. Neotypes are designated for R. hirtipes Osten Sacken and R. solidaginis, and two new species are described—R. gina Dorchin n.sp. and R. guttata Dorchin n.sp. Descriptions include illustrations of galls, male and female morphological characters, and the first description of pupae, where available. New or additional detailed information is also provided on gall structure, phenology, and life history of the gall midges.
... Genetic variation is one key factor underlying trait variations within species (Maddox and Root 1990;Crutsinger et al. 2006;Lamit et al. 2015). For example, genetic variations in the leaf defense traits (Whitham et al. 2006) and in the plant architecture (Crutsinger et al. 2014) underlie the diversity of arthropod and soil microbe communities. ...
Article
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Identifying how variations in functional traits arise is important to predicting the effects of such variations within communities and ecosystems. Here, we evaluated the effects of kin-discrimination on the uptake of soil resources and leaf traits in seedlings of Fagus crenata (Fagaceae). We grew F. crenata seedlings either alone or paired with a sibling or non-sibling, and examined the total biomass, shoot-to-root ratio, leaf traits (chlorophyll content, leaf mass per area, and total contents of phenolic compounds and condensed tannins), and uptake of soil nitrogen, phosphor, and water. In all neighbour treatments, seedlings grew similarly and had similar shoot-to-root ratios. Chlorophyll content and leaf mass per area were higher in plants grown with non-siblings than in those grown alone or with siblings. The total content of phenolic compounds was highest in single seedlings and lowest in non-siblings. Soil moisture was lowest and thus water uptake was highest in plants grown with non-siblings. Our findings suggest that differences in the intensity of competition for soil resources based on kin-discrimination result in differences in leaf traits.
... On the other hand, different consumers may impose selection on different traits, favoring trait integration and increasing genetic constraints. Examples of this include strong genetic covariances in plant 312 resistance to different insect herbivores (Maddox and Root, 1990;Wise, 2007;Wise and Rausher, 2013), although there are also examples where these covariances are weak (Roche and Fritz, 1997;Barbour et al., 2015), or vary from year-to-year (Johnson and Agrawal, 2007). We suggest that 315 gaining predictive insight to the evolutionary consequences of food-web disassembly requires an understanding of the mechanisms governing the assembly of trophic interactions. ...
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Global change is simplifying the structure of ecological networks; however, we are currently in a poor position to predict how these simplified communities will affect the evolutionary potential of remaining populations. Theory on adaptive landscapes provides a framework for predicting how selection constrains phenotypic evolution, but often treats the community context of evolving populations as a "black box". Here, we integrate ecological networks and adaptive landscapes to examine how changes in food-web complexity shape evolutionary constraints. We conducted a field experiment that manipulated the diversity of insect parasitoids (food-web complexity) that were able to impose selection on an insect herbivore. We then measured herbivore survival as a function of three key phenotypic traits. We found that more traits were under selection in simpler vs. more complex food webs. The adaptive landscape was more neutral in complex food webs because different parasitoid species impose different selection pressures, minimizing relative fitness differences among phenotypes. Our results suggest that phenotypic evolution becomes more constrained in simplified food webs. This indicates that the simplification of ecological communities may constrain the adaptive potential of remaining populations to future environmental change.
... It is widely recognized that coevolution between plants and herbivores occurs in a community context (Agrawal, 2005;Johnson and Stinchcombe, 2007;Poelman and Kessler, 2016), but the mechanisms and consequences of such complex interactions are unclear. Most plants must defend against multiple herbivores, often from different feeding guilds (Maddox and Root, 1990;Ali and Agrawal, 2014), which poses a challenge for the plant. In some cases, a single defense trait may be effective against a multitude of herbivores. ...
Article
Full-text available
A major prediction of coevolutionary theory is that plants may target particular herbivores with secondary compounds that are selectively defensive. The highly specialized monarch butterfly (Danaus plexippus) copes well with cardiac glycosides (inhibitors of animal Na+/K+-ATPases) from its milkweed host plants, but selective inhibition of its Na+/K+-ATPase by different compounds has not been previously tested. We applied 17 cardiac glycosides to the D. plexippus-Na+/K+-ATPase and to the more susceptible Na+/K+-ATPases of two non-adapted insects (Euploea core and Schistocerca gregaria). Structural features (e.g., sugar residues) predicted in vitro inhibitory activity and comparison of insect Na+/K+-ATPases revealed that the monarch has evolved a highly resistant enzyme overall. Nonetheless, we found evidence for relative selectivity of individual cardiac glycosides reaching from four to 94-fold differences of inhibition between non-adapted Na+/K+-ATPase and D. plexippus- Na+/K+-ATPase. This toxin-receptor specificity suggests a mechanism how plants could target herbivores selectively and thus provides a strong basis for pairwise coevolutionary interactions between plants and herbivorous insects.
... It is widely recognized that coevolution between plants and herbivores occurs in a community context (Agrawal, 2005;Johnson and Stinchcombe, 2007;Poelman and Kessler, 2016), but the mechanisms and consequences of such complex interactions are unclear. Most plants must defend against multiple herbivores, often from different feeding guilds (Maddox and Root, 1990;Ali and Agrawal, 2014), which poses a challenge for the plant. In some cases, a single defense trait may be effective against a multitude of herbivores. ...
Article
Full-text available
A major prediction of coevolutionary theory is that plants may target particular herbivores with secondary compounds that are selectively defensive. The highly specialized monarch butterfly (Danaus plexippus) copes well with cardiac glycosides (inhibitors of animal Na⁺/K⁺-ATPases) from its milkweed host plants, but selective inhibition of its Na⁺/K⁺-ATPase by different compounds has not been previously tested. We applied 17 cardiac glycosides to the D. plexippus-Na⁺/K⁺-ATPase and to the more susceptible Na⁺/K⁺-ATPases of two non-adapted insects (Euploea core and Schistocerca gregaria). Structural features (e.g., sugar residues) predicted in vitro inhibitory activity and comparison of insect Na⁺/K⁺-ATPases revealed that the monarch has evolved a highly resistant enzyme overall. Nonetheless, we found evidence for relative selectivity of individual cardiac glycosides reaching from 4- to 94-fold differences of inhibition between non-adapted Na⁺/K⁺-ATPase and D. plexippus-Na⁺/K⁺-ATPase. This toxin receptor specificity suggests a mechanism how plants could target herbivores selectively and thus provides a strong basis for pairwise coevolutionary interactions between plants and herbivorous insects.
... Basic genetic information such as this is important for understanding the interactions between goldenrod and its herbivores, which constitute one of the best-studied model systems in plant-herbivore evolutionary ecology (Maddox & Root 1990, Abrahamson & Weis 1997. To that end, I investigated the pattern of inheritance of stem morph in a population of the goldenrod Solidago gigantea Aiton. ...
Article
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Background and aims – For a more complete understanding of the eco-evolutionary dynamics of plant-herbivore interactions, it is important to know the genetic mechanisms that control defence traits, as well as the levels of genetic variation for these traits in plant populations. Here, I present results of a study of the occurrence and pattern of inheritance of the recently discovered trait of ‘resistance-by-ducking’ in the goldenrod Solidago gigantea (Asteraceae). Methods – I grew maternal families of seedlings from fruits collected in a large field population of S. gigantea in southwestern Virginia, USA. I determined stem phenotype (ducking or erect) for 704 plants across 36 maternal families. Key results – Of the 704 plants, 72% had ducking stems and 28% had erect stems. Employing bootstrapping with Hardy-Weinberg principles, I found that the pattern of inheritance was consistent with stem phenotype being controlled by a major gene, with the ducking morph being recessive to the erect morph. The allele frequencies for stem phenotype in the source population were estimated to be 0.85 ducking and 0.15 erect alleles. Conclusions – These findings not only help inform ecological studies of ducking in S. gigantea, but they lay the groundwork for comparative studies of similar goldenrod species whose populations have differing proportions of ducking stems. For example, in all previous studies on populations of S. altissima, ducking stems have been the minority morph, occurring at a frequency of less than 20%. These results suggest that ducking may be costlier in S. altissima, while S. gigantea may face different ecological pressures, or has somehow overcome some of the costs of ducking. © 2018 Meise Botanic Garden and Royal Botanical Society of Belgium.
... In plants, genetic variation can be a key driver of intraspecific trait variation, which in turn can structure species-rich communities of dependent organisms (Crutsinger et al., 2006;Fritz & Price, 1988;Lamit et al., 2015;Maddox & Root, 1990). For example, genetic variation in the leaf chemistry of cottonwoods (Whitham et al., 2006) and in the plant architecture of coyote bush (Crutsinger et al., 2014) have been shown to structure diverse communities of foliar arthropods and soil microbes. ...
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Intraspecific variation can be an important driver of ecological interactions in species‐rich communities. Predicting the effects of intraspecific variation in different environments, however, remains a major challenge. This is because we often do not quantify both the effects of functional traits on associated communities and the extent to which trait variation is due to genetics (genotype effects) vs. plasticity (environment effects). As a consequence, the relative importance of trait plasticity vs. genetic variation in structuring associated communities remains unclear. We sought to fill this gap by conducting common garden experiments with the plant Salix hookeriana across biotic (ant–aphid interactions) and abiotic (wind exposure) environmental gradients in a coastal dune ecosystem. In each experiment, we simultaneously measured plant traits and species richness of associated above‐ and below‐ground communities. We then used statistical models to quantify the relative importance of trait plasticity vs. genetic variation in structuring communities. Our major finding was that trait plasticity was more important than genetic variation in determining the number of species in associated communities. This result was consistent across different environmental contexts (experimental manipulations of ant–aphid interactions and wind exposure), multiple years, and for above‐ground arthropods and root microbes. This occurred because the traits that had the largest effect on species richness were also the most plastic. Synthesis. These results indicate that trait plasticity can be a dominant driver of above‐ and below‐ground biodiversity.
... Error bars are standard error, and different letters represent statistically significant different consumption rates when analyzed using ANOVA. n  8. Invertebrate consumer species differed in their preferences for detritus produced by individual seagrass genotypes, just as for insects on different genotypes of goldenrod (Maddox and Root 1990). Eelgrass genotypes vary in many traits potentially relevant to grazing of live and detrital tissue , Tomas et al. 2011, Reynolds et al. 2016). ...
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Seagrass meadows are among the world's most productive ecosystems, and as in many other systems, genetic diversity is correlated with increased production. However, only a small fraction of seagrass production is directly consumed, and instead much of the secondary production is fueled by the detrital food web. Here, we study the roles of plant genetic diversity and grazer species diversity on detrital consumption in California eelgrass Zostera marina meadows. We used three common mesograzers—an amphipod, Ampithoe lacertosa, an isopod, Idotea resecata, and a polychaete, Platynereis bicaniculata. Each grazer consumed eelgrass detritus at rates greater than live eelgrass or macroalgae. This detrital consumption, however, was not spread evenly over leaves shed from different eelgrass clones. Palatability and consumption varied because of genotype specific differences in leaf texture, secondary metabolites (phenolics), and nutritional quality (nitrogen). Further, detritus derived from some eelgrass genotypes was palatable to all grazers, while detritus from other genotypes was preferentially consumed by only one grazer species. Under monospecific grazer assemblages, plant genetic identity but not diversity influenced detritus consumption. However, more realistic, diverse mesoconsumer communities combined with high plant-detrital genotypic diversity resulted in greater consumption and grazer survival. These results provide a mechanism for field observations of increased mesograzer density and diversity in genetically diverse seagrass assemblages and offer a potential explanation for variation in results of resource diversity-detrital processing experiments in the literature, which often exclude macroinvertebrate taxa. More broadly, our findings support the emerging principle that biodiversity effects are strongest when diversity in both consumer and resource taxa are present.
... Our scale of study will permit an answer to each of these questions, and will be reported in future publications. The scale we use also permits direct comparison with richness on other single plant species which is recorded commonly in community studies: for example , the herbivores on bracken fern around the world (Lawton 1984a, b); the herbivores on Brassica oleracea (Root 1973); milkweed species in the genus Asclepias (Price & Willson 1979); Solidago species (Maddox & Root 1987, 1990); and some savanna legumes (Marques & Price, pers. obs.). ...
Article
Local sampling of larval lepidopterans on Erythroxylum host plant species in tropical (Brazilian) savanna (cerrado) revealed a high species richness with low abundance per species. Cumulative numbers of morphospecies with increasing sampling effort yielded no asymptotic level of richness in sampling periods lasting six, seven and 23 months. Peak richness was reached at 31 species in 1992 and 19 species in 1993, on the three Erthyroxylum species sampled: E. deciduum, E. suberosum, and E. tortuosum. Less than one larvae was found per plant during all sampling times, with a mean of 0.28 species per plants in 1992 and 0.12 in 1993. The number of specimens of all species combined discovered per plant was very low at 0.10 per plant. Many plants remained unattacked on any sampling date with 12%, 8%, and 16% of plants attacked in the species listed in order above. In general, there was an increase in species found during the late dry season when new leaves were produced, but plant phenology seemed to exert only a small influence. Comparable temperate samples indicate a very different assemblage. Richness was from two to over three times higher in the tropics. Number of morphospecies per plant individual was similar at the sites, although total richness was lower in the temperate savanna. Number of total individuals per plants was 11-fold higher in the temperate samples; and the percent of plants with larvae present was over four times higher in the temperate zone (mean of 49%) than in the cerrado (12%). -from Authors
... We assumed that the costs of resistance were manifested through reduced growth, but other sorts of costs have been noted. For instance, when multiple enemies attack a plant species, increasing the resistance to one could increase susceptibility to others (Maddox and Root 1990;Linhart 1991;Simms 1992;Hougen-Eitzman and Rausher 1994;van der Meijden 1996). Although this presents a more complicated situation, the principles of this model should still apply. ...
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We constructed a model to investigate conditions under which intraspecific competition amplifies or diminishes the selective advantage to resistance. The growth trajectories of competing individual plants were depicted by logistic difference equations that incorporated basic costs (lowered growth rate) and benefits (lowered damage) of defense. Analytical results showed that when competition is absent, resistance is favored by high damage, low cost, and slow growth rate. Competition makes selection more complex. When herbivore damage reduces the size of a susceptible plant, resistant neighbors can usurp its resources and thus suppress its regrowth. This competitive interaction amplifies the relative fitness of the resistants. Numerical simulations explored a broader range of conditions. Three factors were varied: competition mode (symmetric vs. asymmetric), resistance type (damage avoidance vs. damage reduction), and timing of attack (early, mid, or late season). We found that competition mode had drastic effects on outcomes. Under symmetric competition, increased plant density intensified the selective advantage of resistance, damage avoidance was more strongly favored than damage reduction, and resistance to late attack was more favored than to early attack. Asymmetric competition had opposite effects: selection acted against resistance at high density, damage reduction was more strongly favored, and resistance against early attack was more favored. Interestingly, the two competition modes induced opposite patterns of density‐dependent selection. The difference between the symmetric and asymmetric cases is explained by the fact that resistance costs during the preattack phase are more strongly amplified by asymmetric competition. When resistance is induced, so that preattack costs of resistance are zero, asymmetric competition more strongly amplified the benefits during the postattack phase. The prediction that selection on resistance will be plant density‐dependent has complex implications for the evolutionary dynamics of defense evolution.
... Goldenrods (Solidago and Euthamia species) are common herbs throughout the eastern United States, which have been studied extensively due to their economic importance as ornamentals, weeds, or sources of pollinators and biological control agents. Hosting a great diversity of herbivorous insects from different feeding guilds (Gagné 1968, McEvoy 1988Maddox & Root 1990;Root & Cappuccino 1992;Fontes et al. 1994), goldenrods have also served as model systems for numerous studies that focused on evolutionary and ecological aspects of speciation, resistance, and tritrophic interactions (e.g., Abrahamson & Weis 1997;Heard et al. 2006;Stireman et al. 2005Stireman et al. , 2006Wise & Abrahamson 2008, Crutsinger et al. 2009). ...
Data
FIGURES 62 – 69. Rhopalomyia leaf and stem galls. Figs. 62 – 64. Rhopalomyia clarkei galls on Solidago rugosa; 62. Young gall. 63. Mature galls. 64. Galls on underside of leaf. 65. Rhopalomyia clarkei galls on stem and leaf of Solidago altissima (photo by M. Wise). Figs. 66 – 67. Rhopalomyia sp. galls on leaves of Solidago gigantea; 66. Very young galls. 67. Mature gall. Figs. 68 – 69. Rhopalomyia gina galls on leaves of Solidago juncea. 68. Gall on upper side of leaf. 69. Tail-like appendage of gall on underside of leaf.
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1. Plant genotype, water stress and their interaction are among the factors contributing to the susceptibility of plants to herbivory. The plant's nitrogen concentration, a critical and often limiting nutrient, differs with plant genotype and water stress. Still, few studies have investigated the impact of the interaction between genotype and water stress on herbivory and plant nitrogen. 2. We established a common garden in Duluth, MN, of tall goldenrod, Solidago altissima, collected from a local Minnesota site to analyse the effects of goldenrod genotype and water stress on leaf nitrogen and the preference and performance of the chrysanthemum lace bug, Corythucha marmorata . 3. Lace bugs had oviposition, nymph and adult preferences among host plant genotypes, water treatments and among genotype and water treatment combinations. Nymph and adult survival and adult mass varied significantly due to plant genotype, water treatment, the interaction between plant and water treatment and the interaction of treatment with lace bug density. Oviposition preference and offspring performance were significantly positively related. 4. Leaf nitrogen increased with the increasing severity of the water limitation in the absence of lace bugs. However, in the presence of lace bugs, there was no difference in nitrogen among water treatments. 5. We hypothesize that lace bugs reduce leaf nitrogen concentration to a lower threshold and then move between plants until nitrogen concentration equalises among all plants.
Preprint
Plant genotype, drought stress, and their interaction are among the factors contributing to the susceptibility of the tall goldenrod, Solidago altissima , to herbivory by the chrysanthemum lace bug, Corythucha marmorata . The plant’s concentration of nitrogen, a critical and often limiting nutrient, differs with plant genotype and drought, but few studies have investigated the impact of the interaction of genotype and drought on herbivory and plant nitrogen. We established a common garden in Duluth, MN, of tall goldenrod collected from a local Minnesota site to analyze the effects of goldenrod genotype and drought on leaf nitrogen and lace bug preference and performance. Lace bugs had oviposition, nymph, and adult preferences among host plant genotypes, drought treatments, and among genotype and drought combinations. Nymph and adult survival and adult weight varied significantly due to plant genotype, drought treatment, the interaction of plant and drought treatment, and the interaction of treatment with lace bug density. Oviposition preference and offspring performance were significantly positively related. Leaf nitrogen increased with the increasing severity of the drought treatment in the absence of lace bugs. However, in the presence of lace bugs, there was no difference in nitrogen among drought treatments. We hypothesize that lace bugs feed on plants until nitrogen concentration reduces to a lower threshold and then move between plants until they have equalized the nitrogen concentration among all plants.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
Chapter
There is increasing evidence that the structure and functioning of ecological communities and ecosystems are strongly influenced by flexible traits of individuals within species. A deep understanding of how trait flexibility alters direct and indirect species interactions is crucial for addressing key issues in basic and applied ecology. This book provides an integrated perspective on the ecological and evolutionary consequences of interactions mediated by flexible species traits across a wide range of systems. It is the first volume synthesizing the rapidly expanding research field of trait-mediated indirect effects and highlights how the conceptual framework of these effects can aid the understanding of evolutionary processes, population dynamics, community structure and stability, and ecosystem function. It not only brings out the importance of this emerging field for basic ecological questions, but also explores the implications of trait-mediated interactions for the conservation of biodiversity and the response of ecosystems to anthropogenic environmental changes.
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Light quality and chemicals in a plant’s environment can provide crucial information about the presence and nature of antagonists, such as competitors and herbivores. Here, we evaluate the roles of three sources of information—shifts in the red:far red (R:FR) ratio of light reflected off of potentially competing neighbors, induced metabolic changes to damage by insect herbivores, and induced changes to volatile organic compounds emitted from herbivore-damaged neighboring plants—to affect metabolic responses in the tall goldenrod, Solidago altissima. We address the hypothesis that plants integrate the information available about competitors and herbivory to optimize metabolic responses to interacting stressors by exposing plants to the different types of environmental information in isolation and combination. We found strong interactions between the exposure to decreased R:FR light ratios and damage on the induction of secondary metabolites (volatile and non-volatile) in plants. Similarly, the perception of VOCs emitted from neighboring plants was altered by the simultaneous exposure to spectral cues from neighbors. These results suggest that plants integrate spectral and chemical environmental cues to change the production and perception of volatile and non-volatile compounds and highlight the role of plant context-dependent metabolic responses in mediating population and community dynamics.
Preprint
Light quality and chemicals in a plant’s environment can provide crucial information about the presence and nature of antagonists, such as competitors and herbivores. Here we evaluate the roles of three sources of information - shifts in the red:far red (FR) ratio of light reflected off of potentially competing neighbors, induced metabolic changes to damage by insect herbivores, and induced changes to volatile organic compounds emitted from herbivore–damaged neighboring plants - to affect metabolic responses in the tall goldenrod, Solidago altissima . We address the hypothesis, that plants integrate the information available about competitors and herbivory to optimize metabolic responses to interacting stressors by exposing plants to the different types of environmental information in isolation and combination. We found strong interactions between the exposure to decreased Red:FR light ratios and damage on the induction of secondary metabolites (volatile and non-volatile) in the receiver plants. Similarly, the perception of VOCs emitted from neighboring plants was altered by the simultaneous exposure to spectral cues from neighbors. These results suggest that plants integrate spectral and chemical environmental cues to change the production and perception of volatile and non-volatile compounds and highlight the role of plant context-dependent metabolic responses in mediating population and community dynamics. Highlight Plants integrate spectral and chemical environmental cues to differentially induce production of volatile and non-volatile compounds
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Aims There is an increasing likelihood that invasive plants are again exposed to their co-evolved specialist herbivores in the non-native range. However, whether there is a latitudinal pattern associated with the resistance of an invasive plant to its co-evolved herbivores and how soil microbes affect resistance has been little explored. We hypothesized that the resistance of invasive Solidago canadensis to its co-evolved insect herbivore Corythucha marmorata could increase with latitude, and that local rhizosphere microbes could facilitate invasive plants to become resistant to their co-evolved herbivores. Methods We conducted a field survey and a greenhouse experiment to examine whether there was a latitudinal pattern in the abundance of C. marmorata and in the damage it caused to S. canadensis in China. We tested whether local rhizosphere microbes of invasive plants can promote the resistance of S. canadensis to C. marmorata herbivory. Important findings In the field survey, both density of C. marmorata and damage level of S. canadensis were positively correlated with latitude, and with S. canadensis plant growth, indicating a latitudinal pattern in the resistance of S. canadensis to C. marmorata. However, in the greenhouse experiment, S. canadensis from different latitudes did not suffer significantly from different levels of damage from C. marmorata. Additionally, the damage level of S. canadensis was lower when rhizosphere soil and rhizomes originated from field S. canadensis with same damage level than with different damage levels. This result indicates that local rhizosphere soil microbes promote the adaptation of S. canadensis to resistance of C. marmorata.
Article
1. Host plant phenotypic traits affect the structure of the associated consumer community and mediate species interactions. Intraspecific variation in host traits is well documented, although a functional understanding of variable traits that drive herbivore community response is lacking. We address this gap by modelling the trait‐environment relationship using insect traits and host plant traits in a multilevel model. 2. We compare herbivore assemblages from the canopy of the phenotypically variable tree Metrosideros polymorpha on Hawai‘i Island. Multiple distinct varieties of M. polymorpha frequently co‐occur, with variation in morphological traits. Using this system, we identify host and insect traits that underlie patterns of herbivore abundance and quantify the strength of host‐insect trait interactions. 3. This work examines plant‐insect interactions at a community scale, across 36 herbivore species in three orders. We find that co‐occurring trees of varying phenotype support distinct communities. Leaf traits, including specific leaf area, trichome presence, and leaf nutrients, explain 46% of variation in insect communities. We find that feeding guild and nymphal life history are correlated with host plant traits, and we show that model predictions are improved by including the host and insect trait interaction. 4. This study demonstrates how insect herbivores traits influence community response to morphologically variable hosts. Environmental heterogeneity indirectly affected herbivore community structure via intraspecific variation in host plants, providing an important source of variation for maintaining diversity in the broader community.
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In novel plant–insect relationships, oviposition preference and nymphal performance determine host range evolution. Corythucha marmorata, native to North America and specialist on asteraceous plants, has been reported to exploit sweet potato (Convolvulaceae) in Japan. Here we examined the capability of females to oviposit and of nymphs to grow on both a conventional host (goldenrod, Solidago altissima) and novel hosts (four sweet potato cultivars), of which the test insects had virtually no experience of contact at the population level. We then tested whether female preference and offspring performance were correlated. Nymphal survival and development time were always significantly greater on goldenrod, followed by sweet potato cultivars Caroline Lea, Benisengan, Narutokintoki, and Beniazuma in that order. Female oviposition preferences showed a similar order. On higher-ranked plants, the females accepted the plant faster and had higher fecundity. When goldenrod was included in the analysis, nymphal development time and survival rate were significantly related to preoviposition period. When goldenrod was excluded, nymphal survival rate was still significantly related to preoviposition period. These results support the theory that females lay their eggs on the most suitable host to maximize offspring fitness, even though C. marmorata had no experience with sweet potato cultivars. As C. marmorata is a hemimetabolous insect, in which adults and nymphs have a similar feeding habit and exploit the same habitat, this relationship seems plausible.
Article
Many plants use terpenoids and other volatile compounds as semiochemicals. Reception of plant volatiles by conspecifics may trigger a defensive phytochemical response. These same compounds can also function as host recognition signals for phytophagous insects. In this experiment, we find that when the specialist gall-forming fly Eurosta solidaginis (Fitch; Diptera: Tephritidae) attacks its tall goldenrod (Solidago altissima (L.; Asterales: Asteraceae)) host plant, the fly indirectly induces a phytochemical response in nearby tall goldenrod plants. This phytochemical response may, in turn, act as a positive signal attracting the goldenrod specialist aphid Uroleucon nigrotuberculatum (Olive; Hemiptera: Aphididae). Laboratory-based experiments exposing ungalled tall goldenrod plants to the volatiles released by E. solidaginis galls demonstrated a consistent increase in foliar terpenoid concentrations in ungalled plants. Analysis of tall goldenrod stem and gall tissue chemistry revealed induction of terpenoids in gall tissue, with a simultaneous decrease in green leaf volatile concentrations. Field experiments demonstrated a consistent spatial relationship in tall goldenrod foliar terpenoid concentrations with distance from an E. solidaginis gall. Both laboratory and field experiments establish consistent induction of the terpene β-farnesene, and that this compound is a strong positive predictor of U. nigrotuberculatum aphid presence on goldenrod plants along with plant biomass and several other foliar terpenoids. These findings suggest E. solidaginis induced phytochemistry, especially β-farnesene, may be acting as a kairomone, driving aphid distribution in the field.
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Nutrient cycling plays a critical role in maintaining biodiversity and ecosystem services in agricultural, urban, and natural lands. However, across landscapes there is substantial unexplained heterogeneity in nutrient cycling. Classic thinking holds that abiotic factors are the source of this spatial heterogeneity with a secondary role of plant biomass. However, recent work suggests that higher trophic levels or variation in traits at the level of plant genotype may also play an important role in structuring nutrient environments. For instance, herbivores may indirectly create heterogeneity in cycling through the induction of chemical and structural changes in plants traits. Phenotypic plasticity due to anti-herbivore defense may then alter nutrient cycling rates by changing the microbial breakdown of plant litter inputs. Alternatively, variation among plant genotypes in the expression of these same traits may overwhelm the influence of phenotypic plasticity on soil processes. Both genetic and environmentally based changes in plant traits have separately been demonstrated to alter soil processes, but their interaction and the relative importance of these sources of variation across local landscapes is unknown. I address this question by developing a plant trait-mediated, conceptual framework of nutrient cycling. I then evaluate this framework within an old-field ecosystem by focusing on the dominant plant species, Solidago altissima, and its dominant grasshopper herbivore, Melanoplus femurrubrum, using a combination of lab assays, a greenhouse pot experiment, a field mesocosm experiment, and field surveys. First, I demonstrate that goldenrod individuals exhibit both genotypic variation and phenotypic plasticity in plant defensive trait responses across a nutrient and herbivory gradient in the greenhouse. At low nutrient supply, genotypes tolerate herbivory (inducing plant physiological changes that decrease the negative impact on fitness) while at high nutrient supply, the same genotypes induce a resistance response detectable through lower herbivore growth rates. These environmentally mediated changes in plant trait expression then altered the ability of a common microbial community to decompose senesced litter harvested from the same plants. Induced resistance in the population of genotypes grown at high nutrient levels led to decreased litter decomposition of herbivore legacy litter. In contrast, at low nutrient supply, herbivore legacy litter decomposed more efficiently compared to control litter. This suggests that the interaction between herbivory and nutrient supply could cause context-dependent acceleration or deceleration of nutrient cycling. As a result, trait plasticity may mediate effects of multiple environmental conditions on ecosystem processes in this system. I tested this hypothesis using a three-year, raised bed, field experiment examining the effect of plasticity and locally relevant genetic variation on ecosystem processes in a naturalistic setting. Genotype clone clusters were planted in homogenized soil in enclosed cages with varying nutrient supply and grasshopper herbivory. Again, I documented strong genetically and environmentally-based trait variation in plant allocation, growth, and leaf traits. I next explicitly linked these genetic and plastic functional trait changes to concurrent changes in a variety of soil processes (microbially available carbon, plant available nitrogen, nitrogen mineralization potential, and microbial biomass) and litter decomposition rates. Importantly, partitioning functional trait variation into genetic and environmental components improved explanatory power. I also documented potential differences in herbivore effects on “slow” vs. “fast” cycling in soil microbially available C pools. Within both experiments the magnitude of trait variation measured was similar to the variation expressed by individuals across a focal field. Taken together, this dissertation demonstrates that plant genotype, herbivores, and nutrients can all modify litter decomposition and other soil processes within ecosystems through differential expression of plant functional traits. Due to the spatially clumped, clonal, and dominant nature of goldenrod, the genetic and herbivory-driven changes documented here could lead to a predictable mosaic of soil process rates across a single old field landscape. This work also highlights the complex interplay between genetically and environmentally-based trait variation in determining population and ecosystem processes within landscapes and improves our understanding of the often-overlooked indirect effects of plant/herbivore interactions on nutrient cycling. It suggests that herbivores may shape not only the evolution of plant populations, but also the soil nutrient environment and microbial community in which plants live. This sets up the potential for eco-evolutionary feedbacks between plant defense expression and soil nutrient availability. More broadly, it suggests that biotic factors, in addition to abiotic ones, play a key role in determining local- scale soil nutrient availability patterns and should potentially be accounted for within ecosystem models. These results are particularly salient in a world where anthropogenic nitrogen inputs continue to rise and climate change is predicted to increase herbivory and thus plant defensive trait induction on landscapes.
Article
We examined phenotypic selection exerted by natural enemies on the gall-making fly Eurosta solidaginis in an extensive field study of 16 populations, spanning four generations. Gall-makers that induce small galls are vulnerable to the attack of Eurytoma gigantea. This imposes upward directional selection on gall size. Insectivorous birds, predominantly the downy woodpecker, are more likely to attack larvae that induce large galls than small ones, and this imposes downward directional selection. We used path analysis to explore the relative contributions of these natural enemies to the net directional selection on gall size. The path models further examined several ecological factors that influence selection intensity through their effects on parasitoid and bird attack rates. Net directional selection varied more strongly with E. gigantea attack than bird attack. Competitive interactions among birds and the three parasitoid species, including E. gigantea, were evidenced by low winter bird attack rates in fields where a high proportion of galls contained the overwintering parasitoids. Eurytoma gigantea attack was heavier in fields where mean gall size was small and bird attack heavier in fields where mean gall size was large. Neither birds nor E. gigantea showed simple density-dependent attack. Data suggested a form of frequency-dependent attack by birds but not by E. gigantea.
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Although there is considerable evidence indicating that herbivory is detrimental to plant fitness, some recent studies of the evolution of plant resistance have concluded that insects do not impose selection on their host plants. A previously untested assumption that underlies most studies of the evolution of plant resistance is that insect distribution patterns are controlled directly by the effects of plant genotype on insect preference and performance. The experiments described here explicitly tested this assumption using the specialist herbivore Uroleucon tissoti (Homoptera: Aphididae) and its host plant Solidago altissima (Asteraceae). Measures of aphid preference and performance were used to predict aphid distribution patterns, and then the predicted distribution patterns were compared with the natural distribution pattern. Although goldenrod genotype had a strong effect on aphid distribution, aphid distribution was not controlled directly by the effect of goldenrod genotype on aphid preference and performance. Instead, a second experiment demonstrated that aphid and spittlebug (Philaenus spumarius and Lepyronia quadrangularis Homoptera: Cercopidae) distribution is controlled largely by genetic variation for resistance to a suite of "branch-causing" herbivores. These herbivores induce branching and aphids and spittlebugs are more abundant on branched plants than unbranched plants. These results indicate that any natural selection imposed by aphids and spittlebugs on goldenrod will depend on the presence or absence of branch-causing herbivores. Thus, selection for plant resistance may depend as much on the assemblage of insect species present as on the identity of each individual species.
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We measured resistance of Salix sericea, the silky willow, to a diverse assemblage of 12 herbivores. We investigated the potential for multispecies coevolution among these herbivores by measuring genetic correlations between pairs of herbivores interacting within the component community. After measuring herbivore attack on half-sib families of potted S. sericea during three years, we found significant narrow-sense heritabilities of resistance to Phyllonorycter salicifoliella and Phyllocnistis sp. in 1991. Thus, there is the potential for selection on resistance to these two herbivores. Despite the many significant phenotypic correlations between herbivore abundances within a year, most genetic correlations between herbivore abundances within a year were not significant. The genetic and phenotypic correlation structure varied from year to year in this three-year study. Thus, it appears that there is the potential for evolution of resistance to the two herbivores for which we found significant heritabilities, but multispecies coevolution seems unlikely.
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Recent theoretical studies have argued that plant-herbivore coevolution proceeds in a diffuse rather than a pairwise manner in multispecies interactions when at least one of two conditions are met: (1) genetic correlations exist between plant resistances to different herbivore species; and (2) ecological interactions between herbivores sharing a host plant cause nonadditive impacts of herbivory on plant fitness. We present results from manipulative field experiments investigating the single and interactive fitness effects of three types of herbivory on scarlet gilia (Ipomopsis aggregata) over two years of study. We utilize these data to test whether selection imposed by herbivore attack on date of first flowering is pairwise (independent) or diffuse (dependent) in nature. Our results reveal complex patterns of the fitness effect of herbivores. Simulated early season browsing had a strong negative fitness effect on plants and also reduced subsequent insect attack. Surprisingly, this ecological interaction did not translate into significant interactions between clipping and insect manipulations on plant fitness. However, we detected a significant interaction between seed fly and caterpillar herbivory on plant fitness, with the negative effect of either insect being greatest when occurring alone. These results suggest that herbivore-imposed selection may have pairwise and diffuse components. In our selection analysis of flowering phenology, we discovered significant pairwise linear selection imposed by clipping, diffuse linear selection imposed by insects, and diffuse nonlinear selection imposed by clipping and insect attack acting simultaneously. Our results reveal that the evolution of flowering phenology in scarlet gilia may be in response to diffuse and pairwise natural selection imposed by multiple herbivores. We discuss the evolution of resistance characters in light of diffuse versus pairwise forms of linear and nonlinear selection and stress the complexity of selection imposed by suites of interacting species.
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Genetic costs of resistance to pathogens may be an important factor maintaining heritable variation for resistance in natural populations. Pleiotropic fitness trade-offs occur when genetic resistance causes reduction in other components of fitness. Although costs of resistance have an important influence on plant-pathogen interactions, few previous studies have detected pleiotropic costs of resistance in the absence of confounding effects of linkage disequilibrium. To avoid this potential problem, we performed artificial selection experiments on resistance to two fungal pathogens, Leptosphaeria maculans, and Peronospora parasitica, and compared growth rates of resistant and susceptible genotypes of Brassica rapa in the absence of pathogens. Leptosphaeria resistance had no effect on growth rate, indicating cost-free defense. In contrast, Peronospora-resistant genotypes grow 6% slower than Peronospora-susceptible genotypes in pathogen-free environments, indicating a significant genetic fitness cost to Peronospora resistance. Such genetic trade-offs could maintain genetic variation in the wild. Another factor that might explain heritable variation for resistance is ecological trade-offs, in which genetic resistance to one species causes susceptibility to another. Such ecological trade-offs do not exist for the pathogens studied in this system.
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Although most plants experience herbivory by several insect species, there has been little empirical work directed toward understanding plant responses to these simultaneous selection pressures. In an experiment in which herbivory by flea beetles (Phyllotreta cruciferae) and diamondback moths (Plutella xylostella) was manipulated in a factorial design, I found that selection for resistance to these herbivores is not independent in Brassica rapa. Specifically, the effect of flea beetle damage on B. rapa fitness depends on the amount of diamondback moth damage a plant experiences: damage by these herbivores has a nonadditive effect on plant fitness. When diamondbacks are abundant, plants that sustain high levels of damage by flea beetles are favored by natural selection, but when diamondbacks are rare, a low level of damage by flea beetles is favored. However, resistance to the later-feeding diamondback moth is not affected by the presence or absence of damage by early-feeding flea beetles. Thus, there are no plant-mediated ecological interactions between these herbivores that affect the outcome of selection for resistance. Because these herbivores do not independently affect plant fitness, neither is likely to develop a pairwise coevolutionary relationship with its host. Instead, coevolution is diffuse.
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Plant communication has been documented in over 35 plant species spanning 16 families to date; however, the underlying mechanisms through which it shapes plants' ecological interactions remain less clear. Using a combination of field/laboratory bioassays, headspace volatile and leaf chemical analyses in tall goldenrod ( Solidago altissima ), we tested the hypothesis that plant‐to‐plant communication affects the performance, feeding and movement behaviour of herbivores by changing plants' chemical phenotypes. We found that plant communication accelerates herbivore movement between host plants while simultaneously reducing herbivory. This suggests that plant communication can limit herbivore loads by keeping herbivores on the move between host plants. We demonstrate that volatile chemicals emitted from herbivore‐attacked plants are sufficient to explain metabolic responses in and ecological consequences for the exposed neighbour plant. Volatile profiles of beetle ( Trirhabda virgata )‐damaged and undamaged plants show substantial compositional differences, especially in sesquiterpene emission, indicating that these differences have the potential to provide neighbouring plants with specific information about herbivores in the vicinity. Despite qualitative and phenological differences in plants' metabolic responses to herbivory‐induced volatile organic compounds ( VOC s) and feeding herbivores, herbivores nonetheless respond similarly to directly damaged plants and plants exposed to VOC s from damaged neighbours as if they were of equivalently poor quality. This study suggests that by enlarging the spatial scale at which induced resistance affects the distribution of plant chemical phenotypes in plant populations, VOC ‐mediated plant communication alters the movement behaviour and performance of herbivores. A lay summary is available for this article.
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Examined Eurosta solidaginis host choice among 38 naturally occurring clones of tall goldenrod Solidago altissima. Significant variation was found in the percentages of ramets ovipunctured, punctured ramets with eggs, ramets galled, and punctured ramets that formed galls. All genotypes of S. altissima are not equally suitable (capable of supporting larval development) and/or acceptable (having the proper cues to stimulate oviposition). Significantly more larval mortality occurred in the meristems of resistant clones than in the meristems of susceptible clones; 73% of dead Eurosta larvae were surrounded by necrotic plant tissue, apparently due to a hypersensitive response by the plant to the gallmaker's stimulus. -from Authors
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Seed dispersal and seedling emergence of common taxa growing in a Solidago-dominated old field in central New York (USA) were monitored from May 1982 to June 1984. Over 3.5x104 seeds per m2 were captured on seed traps in each of the two years, with peaks occuring in July (due to Hieracium) and in November (due to Solidago). About 4.0x103 seedling/m2 emerged beneath the intact community in each of the two years. Although seedlings emerged predominantly in the early spring, a secondary peak occurred in September and October when many seedlings of introduced grasses appeared. Two additional aspects of the reproductive biology of the major taxa were related to the seasonal timing of seed dispersal: As the date of peak seed dispersal (among taxa) became progressively later in the season, (1) the duration of dispersal increased from about one week to about one-half year, and (2) the delay between the peak of seed dispersal and the peak of seedling emergence increased from a few days to about one-half year.
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The densities of four species of gall-forming sawflies were found to vary significantly among willow host plant clones. Two of the speices varied among host plants at four sites in each of three years. The other two species varied in density among host plants at most of the sites in two of the three years. Total sawfly density also varied significantly among clones. Individual species densities on willow clones were significantly positively correlated between years when all sites were combined and frequently when sites were considered separately. Most pairwise species combinations were independent in density between years, but some negative correlations existed between the stem galler and the leaf galler. Gall-former densities also were largely independent among clones within years with all sites combined and with sites considered separately. The significant correlations were nearly all positive. At all four sites the combination of significant variation in sawfly densities among willow clones in the field and independence of species densities among clones resulted in significantly different communities (relative abundance of species) among willow clones in three years. Although sawfly abundances differed substantially among the four sites, this remained true. It is argued that the pattern of community structure among clones is the result of variation in host plant quality of clones. We propose an hypothesis to account for patterns of herbivore species associations based on intrapopulation host plant variation.
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Genetic variation in resistance to 16 species of herbivorous insects was studied in 18 clones of Solidago altissima growing in an old field near Ithaca, New York, USA. Resistance to each insect, defined as the abundance of a species attacking a particular host genotype relative to other genotypes, was measured in both the natural stand and in two experimental gardens. The heritability of resistance was estimated by parent-offspring regression and sibcorrelation. The primary result was that clones differed in resistance to 15 of 16 insect species. The resistance of genotypes to these insect species remained relatively constant over the four years of the study. However, for only 10 of these resistances were the heritability estimates significantly different from zero. Thus the common assumption of plant-insect studies — that phenotypic variation in insect abundance is closely correlated with underlying genetic variation — is only conditionally true. There is heritable variation in resistance to many insects, but not all. The insects for which we observed heritable variation in plant resistance represent five different orders and several functional groups, including leaf chewers, phloem and xylem feeders, and gall formers. There was no apparent pattern between the degree of heritability of plant resistance and the destructiveness, feeding method, breadth of host range, or taxonomic group of the insects. The lack of marked heritable variation in resistance to some insects may be the result of (a) reduced variation caused by strong selection during prolonged or repeated insect outbreaks, and (b) genotype-environment interactions that obscure differences among genotypes.
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The effects of both genotype and spatial position of host plants on density, proportion, and total community structure of herbivore species were experimentally tested for a guild of gall-forming sawflies on their host plant, arroyo willow Salix lasiolepis. Between 20-50% of variation in density of the stem galler Euura lasiolepis and the leaf folder Phyllocolpa sp., was due to clone genotype, whereas only 9-28% of variation in the density of the leaf galler Pontania sp. and the petiole galler Euura sp. was due to clone genotype. Plant morphological traits that are important to sawfly oviposition in the field (eg mean shoot length) differed significantly among willow clones and were correlated with variation in density of 3 of the 4 sawfly species. -from Authors
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Each individual of a multivariate sample may be represented by a point in a multidimensional Euclidean space. Cluster analysis attempts to group these points into disjoint sets which it is hoped will correspond to marked features of the sample. Different methods of cluster analysis of the same sample may assume different geometrical distributions of the points or may employ different clustering criteria or may differ in both respects. Three superficially different methods of cluster analysis are examined. It is shown that the clustering criteria of all these methods, and several new ones derived from or suggested by these methods, can be interpreted in terms of the distances between the centroids of the clusters; the geometrical point distribution is found in most instances. The methods are compared, suggestions made for their improvement, and some of their properties are established.