PAIRWISE VERSUS DIFFUSE NATURAL SELECTION AND THE MULTIPLE HERBIVORES OF SCARLET GILIA,IPOMOPSIS AGGREGATA

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.     

THE EVOLUTION OF RESISTANCE TO HERBIVORY IN IPOMOEA PURPUREA. II. NATURAL SELECTION BY INSECTS AND COSTS OF RESISTANCE

An important component of the process of coevolution between plants and their insect herbivores is the imposition of selection on plants by insects. Although such selection has been inferred from indirect evidence, little direct evidence for it exists. One goal of this study was to seek direct evidence by determining, for a single plant-herbivore system, whether insect herbivores impose selection on their host plants. A second goal was to determine whether costs are associated with genotypes that confer resistance to herbivores, as has been commonly postulated. The annual morning glory, Ipomoea purpurea, exhibits genetic variation in resistance to four different types of insects. For three of these types, most of the genetic variation is additive. Removal of insect herbivores increased the number of seeds produced by I. purpurea by 20% and eliminated additive genetic variation for seed number (fitness). This result implies that herbivores impose selection on some trait(s) of their host plants. Coupled with selection for decreased damage by corn earworms, as revealed by a negative additive genetic covariance between damage and fitness, this result suggests that insect herbivores impose selection on resistance to corn earworms in I. purpurea. Two types of cost of resistance to herbivores were sought in I. purpurea: 1) internal trade-offs in allocation of resources and 2) ecological trade-offs between resistances to different insects. No costs of either type were detected. This result suggests that cost-benefit arguments that attempt to predict the evolution of levels of resistance to herbivores are not applicable to I. purpurea.     

Niches and size relationships in Coleoptera associated with Cardueae host plants: adaptations to resource gradients

Summary The ecological meaning of size relationships within guilds is still a matter of debate. We analyzed the niches and size relationships in Coleoptera associated with Cardueae host plants. Species were grouped into guilds using distributional data, host records and feeding strategies: a) The species of the genus Larinus are inhabitants of flower heads within the Cynaroideae. Two types of Larinus species were distinguished: one type attacks immature flower heads, the other exploits the floer heads in a more advanced stage. The females of the first group have elongated rostres adapted to piercing through the bracts of closed flower heads, the other group possesses blunt, short rostres. For an oligophagous group of four Larinus species we are able to show that the distribution of average female rostre length is non-random. b) In southern France four stem boring species of the genera Agapanthia and Lixus coexist within the same hosts. The frequency distributions of body length from these species are clearly overdispersed. c) Coexisting species of the folivorous genus Cassida show no differences in body sizes. We conclude that morphometric differences within the investigated guild of endophytic species (Larinus and Agapanthia/Lixus) evolved in response to size of the used plant structures and the size of potentially competing species, a pattern not evident in ectophytic species. We suggest that these differences are part of a general pattern as the evolution of herbivorous guild may strongly depend on the way how the host resource is exploited (endophagy vs ectophagy). So current differences in statements on the organization of herbivore communities could perhaps be reconciled.     

History of exposure to herbivores increases the compensatory ability of an invasive plant

Release from natural enemies is frequently cited as an important factor contributing to plant invasions. But such effects are likely to be temporary—native herbivores can form new plant-herbivore associations and co-evolved insects might reach the new range. While the potential effects of the initial enemy release have been well studied, the consequences of any resumption of herbivory are poorly understood. Alternanthera philoxeroides is one of the most widespread invasive plants in China and is attacked both by a specialist herbivore introduced from the native range, Agasicles hygrophila, and a native beetle Cassida piperata Hope which has formed a new association. However, these insects are not found throughout the invaded range. To test the effect of the history of population exposure to herbivory on compensatory ability, plants were cultured from 14 populations around China that differed in whether A. hygrophila or C. piperata were present. Treatment plants were exposed to herbivory by A. hygrophila for a week until 50% of the leaf area was defoliated, then grown for 80 days. Plants from populations with prior exposure to herbivory (of any kind) accumulated more root mass than populations without prior exposure, indicating that prior exposure to insects can stimulate plant compensation to herbivory. We would recommend that potential changes in plant tolerance in response to prior exposure to herbivory are considered in invasive plant management plans that employ bio-control agents.     

Herbivorous insects reduce growth and reproduction of big sagebrush (<Emphasis Type="Italic">Artemisia tridentata</Emphasis>)

Insect herbivores can reduce growth, seed production, and population dynamics of host plants, but do not always do so. Big sagebrush (Artemisia tridentata) has one of the largest ranges of any shrub in North America, and is the dominant and characteristic shrub of the extensive sagebrush steppe ecosystem of the western United States. Nevertheless, the impact of insect herbivores on big sagebrush, its dominant and characteristic shrub, is largely unknown. Occasional large effects of insect herbivore outbreaks are documented, but there is little knowledge of the impact of the more typical, nominal herbivory that is produced by the diverse community of insects associated with big sagebrush in natural communities. In 2008, we removed insects from big sagebrush plants with insecticide to evaluate whether insect herbivores reduced growth and seed production of big sagebrush. Removal of herbivores led to significant and substantial increases in inflorescence growth (22%), flower production (325%), and seed production (1053%) of big sagebrush. Our results showed the impact of insect herbivory in the current growing season on the growth and reproduction of big sagebrush and revealed an unrecognized, significant role of non-outbreak herbivores on big sagebrush.     

Effects of nonhost and host plants on insect herbivory covarying with plant size in the cruciferous plant <Emphasis Type="Italic">Turritis glabra</Emphasis>

Correlation between plant size and reproductive output may be modified by herbivory in accordance with host plant density and the presence of nonhost plants. To elucidate the effects of nonhost plant density and host plant density on the intensity of herbivory and reproductive output of the host plant in relation to plant size under natural conditions, we investigated the abundance of three lepidopteran insects, Plutella maculipennis, Anthocharis scolymus, and Pieris rapae the intensity of herbivory, and fruit set of their host plant, Turritis glabra (Cruciferae). To elucidate the effects of nonhost and host plant density, we selected four categories of plots under natural conditions: low density of nonhost and high density of host plants; low density of both nonhost and host plants; high density of both nonhost and host plants; and high density of nonhost and low density of host plants. The plant size indicated by stem diameter was a good predictor of the abundance of all herbivorous species. The effects of density of nonhost and host plants on the abundance of insects varied among species and stages of insects. As the abundance of insects affected the intensity of herbivory, herbivory was more apparent on larger host plants in plots with low density of both nonhost and host plants. Consequently, the correlation between plant size and the number of fruits disappeared in low plots with density of both nonhost and host plants. In this T. glabra– herbivorous insect system, the density of nonhost plants and host plants plays an important role in modifying the relationship between plants and herbivores under natural conditions. Received: July 19, 1999 / Accepted: June 15, 2000     

Insect herbivores as potential causes of mortality and adaptation in gallforming insects

Summary Recent studies have suggested that plant galls benefit only the insects living in them and not the host plants, and that galls are induced by insects primarily to improve the plant as a microenvironment or a food source. The potential advantage to insects of protection from their predators and parasitoids has been considered unclear and perhaps minor in importance. However, the potential threat to gallforming insects from other insect herbivores has usually been relatively neglected. This paper notes literature and observations which suggest that herbivores may either consume or be deterred by galls. Even soft leaf galls produced by Hormaphis and Phylloxera aphids appeared to deter some herbivores in the field. The threat of herbivory to galls might help explain general patterns of gall ecology and morphology, and deserves closer attention.     

Increased herbivory but not cyanogenesis is associated with urbanization in a tropical wildflower

Urbanization is associated with numerous changes to the biotic and abiotic environments, many of which lead to a loss of biodiversity. Some studies have documented increased herbivory rates in cities, which has been hypothesized to lead to the evolution of novel defence traits in plants. Yet evidence supporting this hypothesis is contradictory and entirely absent from South American cities. To address this research gap, we evaluated herbivory rates in the native urban wildflower, Turnera subulata (Turneraceae), along an urbanization gradient in Joao Pessoa, Brazil. We predicted that higher rates of herbivory in cities would lead to the expression of cyanogenesis, a chemical defence found in a closely related Turnera species. We estimated herbivory rates and screened for cyanogenesis in 32 populations along the urbanization gradient, quantified by the Human Footprint Index and the amount of impervious surface surrounding each site. We found herbivory rates increased in T. subulata populations with increasing urbanization, but we did not find evidence of cyanogenesis in any of the populations. Our results suggest that although herbivores respond positively to urbanization, the fitness effects of leaf herbivory may be insufficient to select for the evolution of cyanogenesis in some plants. Our results provide valuable insight into the effects of urbanization on plant-herbivore interactions in the tropics.     

Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae

Predicting the host range for herbivores has been a major aim of research into plant-herbivore interactions and an important model system for understanding the evolution of feeding specialization. Among many terrestrial insects, host range is strongly affected by herbivore phylogeny and long historical associations between particular herbivore and plant taxa. For small herbivores in marine environments, it is known that the evolution of host use is sculpted by several ecological factors (e.g., food quality, value as a refuge from predators, and abiotic forces), but the potential for phylogenetic constraints on host use remains largely unexplored. Here, we analyze reports of host use of herbivorous amphipods from the family Ampithoidae (102 amphipod species from 12 genera) to test the hypotheses that host breadth and composition vary among herbivore lineages, and to quantify the extent to which nonpolar secondary metabolites mediate these patterns. The family as a whole, and most individual species, are found on a wide variety of macroalgae and seagrasses. Despite this polyphagous host use, amphipod genera consistently differed in host range and composition. As an example, the genus Peramphithoe rarely use available macrophytes in the order Dictyotales (e.g., Dictyota) and as a consequence, display a more restricted host range than do other genera (e.g., Ampithoe, Cymadusa, or Exampithoe). The strong phylogenetic effect on host use was independent of the uneven distribution of host taxa among geographic regions. Algae that produced nonpolar secondary metabolites were colonized by higher numbers of amphipod species relative to chemically poor genera, consistent with the notion that secondary metabolites do not provide algae an escape from amphipod herbivory. In contrast to patterns described for some groups of phytophagous insects, marine amphipods that use chemically rich algae tended to have broader, not narrower, host ranges. This result suggests that an evolutionary advantage to metabolite tolerance in marine amphipods may be that it increases the availability of appropriate algal hosts (i.e., enlarges the resource base).     

Misleading herbivory in a tropical tree

The damage caused by herbivores can be confused with the drop of necrotic spots due to hypersensitive reactions. The negative impact of sessile herbivores on host plants is minimized by hypersensitive reactions that result in the death of attacked tissue. We reported a phenomenon that remarkably resembles herbivore damage, but is in fact a reaction to endophytic herbivores or pathogens. Although the damages on Tapirira guianensis leaves (Anacardiaceae) appear to be chew marks from herbivores, they are in fact dropped necrotic spots caused by gall-inducing insects. The phenomenon is widespread and challenges the view that gall-inducing insects inflict less damage on host plants, which was previously stated according to the rates of herbivory inflicted by free-feeding herbivores. The study highlights the need to reassess the past evaluations for some plant species, as they may have overestimated herbivory rates.     

Interactions among fungal endophytes,grasses and herbivores

The interaction between two species often depends on the presence or absence of a third species. One widespread three-species interaction involves fungal endophytes infecting grasses and the herbivores that feed upon them. The endophytes are allied with the fungal family Clavicipitaceae and grow systemically in intercellular spaces in above-ground plant tissues including seeds. Like relatedClaviceps species, the endophytes produce a variety of alkaloids that make the host plants toxic or distasteful to herbivores. A large number of grass species are infected, especially cool-season grasses in temperate areas. Field and laboratory studies have shown that herbivores avoid infected plants in choice trials and suffer increased mortality and decreased growth on infected grasses in feeding experiments. Resistance to herbivores may provide a selective advantage to infected plants in competitive interactions with noninfected plants. Recent studies have shown that differential herbivory can reverse competitive hierarchies among plant species. Both endophyte-infected and noninfected tall fescue grass (Festuca arundinacea) are outcompeted by orchardgrass (Dactylis glomerata) in the absence of insect herbivory. However, when herbivores are present infected tall fescue outcompetes orchardgrass. These results suggest that the frequency of infection in grass species and grassland communities will increase over time. Several studies are reviewed illustrating increases in infection frequency within grass populations subject to herbivore pressure. Endophytic fungi may be important regulators of plant-herbivore interactions and so indirectly affect the structure and dynamics of plant communities.     

Does mother know best? The preference–performance hypothesis and parent–offspring conflict in aboveground–belowground herbivore life cycles

1. A substantial amount of research on host‐plant selection by insect herbivores is focused around the preference–performance hypothesis (PPH). To date, the majority of studies have primarily considered insects with aboveground life cycles, overlooking insect herbivores that have both aboveground and belowground life stages, for which the PPH could be equally applicable. 2. This study investigated the factors influencing the performance of the root‐feeding vine weevil (Otiorhynchus sulcatus) larvae and whether this was linked to the oviposition behaviour of the maternal adult living aboveground. 3. Maternal insects feeding aboveground reduced root biomass by 34% and increased root carbon by 4%. Larvae feeding on plants subjected to aboveground herbivory had reduced mass. Irrespective of the presence of maternal herbivory, larval mass was positively correlated with root biomass. 4. Larval mass was also reduced by conspecific larvae, previously feeding on roots (19% reduction). However, the mechanism underpinning this effect remains unclear, as in contrast to maternal herbivory aboveground, prior larval feeding did not significantly affect root biomass or root carbon concentrations. 5. Maternal insects did not distinguish between plants infested with larvae and those that were free of larvae, in terms of their egg‐laying behaviour. Conversely, maternal insects tended to lay eggs on plants with smaller root systems, a behaviour that is likely to negatively affect offspring performance. 6. The PPH is not supported by our findings for the polyphagous vine weevil feeding on the host plant raspberry (Rubus idaeus), and in fact our results suggest that there is the potential for strong parent–offspring conflict in this system.     

Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: Prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation

Background  

Using phylogenetic approaches, the expectation that parallel cladogenesis should occur between parasites and hosts has been validated in some studies, but most others provided evidence for frequent host shifts. Here we examine the evolutionary history of the association between Microbotryum fungi that cause anther smut disease and their Caryophyllaceous hosts. We investigated the congruence between host and parasite phylogenies, inferred cospeciation events and host shifts, and assessed whether geography or plant ecology could have facilitated the putative host shifts identified.     

Can the evolution of plant defense lead to plant-herbivore mutualism?

Moderate rates of herbivory can enhance primary production. This hypothesis has led to a controversy as to whether such positive effects can result in mutualistic interactions between plants and herbivores. We present a model for the ecology and evolution of plant-herbivore systems to address this question. In this model, herbivores have a positive indirect effect on plants through recycling of a limiting nutrient. Plants can evolve but are constrained by a trade-off between growth and antiherbivore defense. Although evolution generally does not lead to optimal plant performance, our evolutionary analysis shows that, under certain conditions, the plant-herbivore interaction can be considered mutualistic. This requires in particular that herbivores efficiently recycle nutrients and that plant reproduction be positively correlated with primary production. We emphasize that two different definitions of mutualism need to be distinguished. A first ecological definition of mutualism is based on the short-term response of plants to herbivore removal, whereas a second evolutionary definition rests on the long-term response of plants to herbivore removal, allowing plants to adapt to the absence of herbivores. The conditions for an evolutionary mutualism are more stringent than those for an ecological mutualism. A particularly counterintuitive result is that higher herbivore recycling efficiency results both in increased plant benefits and in the evolution of increased plant defense. Thus, antagonistic evolution occurs within a mutualistic interaction.     

Host range in phytophagous insects: the potential role of generalist predators

Summary The potential role of generalist natural enemies is presented as one of the important ecological pressures that select for narrow host range in phytophagous insects, and dominant relative to physiological bases for specialization. Experiments are described in three completely different systems indicating that generalist herbivores are more vulnerable to predation than specialist herbivores. The three predators were (a) the vespid waspMischocyttarus flavitarsus, (b) the Argentine antIridomyrmex humilis and (c) the coccinellid beetleHippodamia convergens. It is concluded the predators may provide strong selection pressure for maintenance and perhaps evolution of narrow host range in insect herbivores.     

Colonization of a host tree by herbivorous insects under a changing climate

Climate warming has been predicted to increase the abundance of herbivorous insects. Together with concurrent poleward shifts in many insect species this may increase herbivore pressure on plants. However, the manner in which plants at higher latitudes become colonized by herbivorous insects in the future is unknown. We established a translocation experiment using 26 micropropagated silver birch Betula pendula genotypes from six populations originating from 60°N to 67°N, to study the susceptibility of the translocated birches to local herbivores. The birches were planted at three different latitudes in Finland (60°N, 62°N and 67°N). We studied the effect of source population and latitudinal translocation on herbivore density, species richness, and community composition among the genotypes growing in the same environmental conditions in two years; 2011 and 2012. The source population explained the variation in the herbivore density only in 2012, whereas latitudinal translocation did not affect herbivore density. Variation in species richness was not explained by the source population or by the latitudinal translocation. At two of the study sites, the similarity of the herbivore communities among the populations decreased with increasing latitudinal distance of the source populations, possibly because birch populations that grow geographically closer to each other are genetically more similar, and therefore support a more similar composition of the arthropod community. All birch genotypes were colonized by local herbivores, suggesting that as herbivores shift their ranges polewards, they are able to colonize novel host‐plant genotypes. This enables compositional changes in insect communities on their host plants in the future, which in turn, might affect total herbivory and eventually, plant growth.     

Comparative analysis of quantitative trait loci controlling glucosinolates,myrosinase and insect resistance in Arabidopsis thaliana

Evolutionary interactions among insect herbivores and plant chemical defenses have generated systems where plant compounds have opposing fitness consequences for host plants, depending on attack by various insect herbivores. This interplay complicates understanding of fitness costs and benefits of plant chemical defenses. We are studying the role of the glucosinolate-myrosinase chemical defense system in protecting Arabidopsis thaliana from specialist and generalist insect herbivory. We used two Arabidopsis recombinant inbred populations in which we had previously mapped QTL controlling variation in the glucosinolate-myrosinase system. In this study we mapped QTL controlling resistance to specialist (Plutella xylostella) and generalist (Trichoplusia ni) herbivores. We identified a number of QTL that are specific to one herbivore or the other, as well as a single QTL that controls resistance to both insects. Comparison of QTL for herbivory, glucosinolates, and myrosinase showed that T. ni herbivory is strongly deterred by higher glucosinolate levels, faster breakdown rates, and specific chemical structures. In contrast, P. xylostella herbivory is uncorrelated with variation in the glucosinolate-myrosinase system. This agrees with evolutionary theory stating that specialist insects may overcome host plant chemical defenses, whereas generalists will be sensitive to these same defenses.     

Combined Effects of Extreme Climatic Events and Elevation on Nutritional Quality and Herbivory of Alpine Plants

Climatic extreme events can cause the shift or disruption of plant-insect interactions due to altered plant quality, e.g. leaf carbon to nitrogen ratios, and phenology. However, the response of plant-herbivore interactions to extreme events and climatic gradients has been rarely studied, although climatic extremes will increase in frequency and intensity in the future and insect herbivores represent a highly diverse and functionally important group. We set up a replicated climate change experiment along elevational gradients in the German Alps to study the responses of three plant guilds and their herbivory by insects to extreme events (extreme drought, advanced and delayed snowmelt) versus control plots under different climatic conditions on 15 grassland sites. Our results indicate that elevational shifts in CN (carbon to nitrogen) ratios and herbivory depend on plant guild and season. CN ratios increased with altitude for grasses, but decreased for legumes and other forbs. In contrast to our hypotheses, extreme climatic events did not significantly affect CN ratios and herbivory. Thus, our study indicates that nutritional quality of plants and antagonistic interactions with insect herbivores are robust against seasonal climatic extremes. Across the three functional plant guilds, herbivory increased with nitrogen concentrations. Further, increased CN ratios indicate a reduction in nutritional plant quality with advancing season. Although our results revealed no direct effects of extreme climatic events, the opposing responses of plant guilds along elevation imply that competitive interactions within plant communities might change under future climates, with unknown consequences for plant-herbivore interactions and plant community composition.     

Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Benevolent herbivores?

Two questions dominate current thinking on plant-herbivore interactions: what is the impact of feeding by herbivores on the distribution and abundance of plants; and what is the role of herbivory as an agency of natural selection, leading to differential performance of host plant genotypes? These two questions come together in discussions of how the evolutionary consequences of herbivory are manifest at the population and ecosystem levels.