When is a herbivore not a herbivore?

Summary Young herbivores are not herbivores. With the apparent exception of some chewing insects they cannot survive and growth without eating animal or microbial protein. Further reinforcing how short available nitrogen is in plant food, adult herbivores must feed selectively and depend on intestinal microorganisms to obtain sufficient nitrogen for maintenance and breeding.     

Induced plant defenses breached? Phytochemical induction protects an herbivore from disease

Although wound-induced responses in plants are widespread, neither the ecological nor the evolutionary significance of phytochemical induction is clear. Several studies have shown, for example, that induced responses can act against both plant pathogens and herbivores simultaneously. We present the first evidence that phytochemical induction can inhibit a pathogen of the herbivore responsible for the defoliation. In 1990, we generated leaf damage by enclosing gypsy moth larvae on branches of red oak trees. We then inoculated a second cohort of larvae with a nuclear polyhedrosis virus (LdNPV) on foliage from the damaged branches. Larvae were less susceptible to virus consumed on foliage from branches with increasing levels of defoliation, and with higher concentrations of gallotannin. Defoliation itself was not related to any of our chemistry measures. Field sampling supported the results of our experiments: death from virus among feral larvae collected from unmanipulated trees was also negatively correlated with defoliation. In 1991, defoliation and gallotannin were again found to inhibit the virus. In addition, gallotannin concentrations were found to be positively correlated with defoliation the previous year. Compared with previous results that demonstrated a delecterious effect of induction on gypsy moth pupal weight and fecundity, the inhibition of the virus should confer an advantage to the gypsy moth. Since leaf damage levels increase as gypsy moth density increases, and since leaf damage inhibits the gypsy moth virus, there is the potential for positive feedback in the system. If phytochemical induction in red oak can inhibit an animal pathogen such as LdNPV, it suggests to us that induction in red oak is a generalized response to tissue damage rather than an adaptive defense against herbivores.     

Cyanide detoxification in an insect herbivore: Molecular identification of β-cyanoalanine synthases from Pieris rapae

Cyanogenic compounds occur widely in the plant kingdom. Therefore, many herbivores are adapted to the presence of these compounds in their diet by either avoiding cyanide release or by efficient cyanide detoxification mechanisms. The mechanisms of adaptation are not fully understood. Larvae of Pieris rapae (Lepidoptera: Pieridae) are specialist herbivores on glucosinolate-containing plants. They are exposed to cyanide during metabolism of phenylacetonitrile, a product of benzylglucosinolate breakdown catalyzed by plant myrosinases and larval nitrile-specifier protein (NSP) in the gut. Cyanide is metabolized to β-cyanoalanine and thiocyanate in the larvae. Here, we demonstrate that larvae of P. rapae possess β-cyanoalanine activity in their gut. We have identified three gut-expressed cDNAs designated PrBSAS1-PrBSAS3 which encode proteins with similarity to β-substituted alanine synthases (BSAS). Characterization of recombinant PrBSAS1-PrBSAS3 shows that they possess β-cyanoalanine activity. In phylogenetic trees, PrBSAS1-PrBSAS3, the first characterized insect BSAS, group together with a characterized mite β-cyanoalanine synthase and bacterial enzymes indicating a similar evolutionary history.     

Introduction: Plant–herbivore interactions

This special feature resulted from a symposium entitled "Interactions Between Plants and Their Herbivores," held during the Meeting of the Society of Population Ecology in Ohmi-Shirahama, Shiga, Japan, in October 1999 (Chairperson of Symposium: Professor Emeritus E. Kuno of Kyoto University). This theme emerged from discussions by the organizing committee for this symposium: N. Yamamura, J. Takabayashi, T. Nishida, and N. Ohsaki. Professor Mark D. Rausher of Duke University was invited as a special lecturer. In this series of reports, five of the seven participants illustrate the variation found in plant–herbivore interactions and address some problems inherent in current theory.     

Thresholds in plant–herbivore interactions: predicting plant mortality due to herbivore browse damage

Patterns of herbivore browse at small scales, such as the rate of leaf consumption or plant preferences, drive the impact of herbivores on whole-plant processes, such as growth or survival, and subsequent changes in plant population structure. However, herbivore impacts are often non-linear, highly variable and context-dependent. Understanding the effect of herbivores on plant populations therefore requires a detailed understanding of the relationships that drive small-scale processes, and how these interact to generate dynamics at larger scales. We derive a mathematical model to predict annual rates of browse-induced tree mortality. We model individual plant mortality as a result of rates of foliage production, turnover and herbivore intake, and extend the model to the population scale by allowing for between-tree variation in levels of herbivore browse. The model is configurable for any broadleaved tree species subject to vertebrate or invertebrate browse, and is designed to be parameterized from field data typically collected as part of browse damage assessments. We parameterized and tested the model using data on foliage cover and browse damage recorded on kamahi trees (Weinmannia racemosa) browsed by possums (Trichosurus vulpecula) in New Zealand forests. The model replicated observed patterns of tree mortality at 12 independent validation sites with a wide range of herbivore densities and browse damage. The model reveals two key thresholds; in plant foliar cover, indicating when individual trees may be at high risk from browse-induced mortality, and in herbivore intake, leading to high rates of mortality across the whole population.     

Can an herbivore affect where a top predator kills its prey by modifying woody vegetation structure?

In large mammal communities, little is known about modification of interspecific interactions through habitat structure changes. We assessed the effects of African elephants (Loxodonta africana) on features of woody habitat structure that can affect predator–prey interactions. We then explored how this can influence where African lions (Panthera leo) kill their prey. Indeed, lions are stalk-and-ambush predators and habitat structure and concealment opportunities are assumed to influence their hunting success. During 2 years, in Hwange National Park, Zimbabwe, kill sites (n = 167) of GPS-collared lions were characterized (visibility distance for large mammals, distance to a potential ambush site and presence of elephant impacts). We compared characteristics of lion kill sites with characteristics of random sites (1) at a large scale (i.e. in areas intensively used by lions, n = 418) and (2) at the microhabitat scale (i.e. in the direct surrounding available habitat, < 150 m, n = 167). Elephant-impacted sites had a slightly higher visibility and a longer distance to a potential ambush site than non-impacted sites, but these relationships were characterized by a high variability. At large scale, kill sites were characterized by higher levels of elephant impacts compared to random sites. At microhabitat scale, compared to the direct nearby available habitat, kill sites were characterized by a reduced distance to a potential ambush site. We suggest a conceptual framework whereby the relative importance of habitat features and prey abundance could change upon the scale considered.     

Structure of a herbivore–parasitoid community: Are parasitoids shared by different herbivore guilds?

Plant–herbivore–parasitoid interactions are a common occurrence in terrestrial food webs. Few parasitoids are thought to be shared by host insects of different feeding guilds because different parasitism strategies are required to use hosts of different feeding types. However, this assumption has rarely been tested using data from nature. To clarify whether parasitoids are shared among host guilds, I examined the structure of parasitoid communities on herbivore guilds associated with two Rhododendron species (Ericaceae) in a temperate secondary forest in central Japan. Leaf- and flower-feeding insects were collected from Rhododendron reticulatum and Rhododendron macrosepalum shrubs and reared in the laboratory for 3 years from April 1999 to March 2002. In total, 79 species of holometabolous herbivores (Lepidoptera, Diptera, Coleoptera, and Hymenoptera) were recorded, with 62 species on R. reticulatum and 51 species on R. macrosepalum. A total of 81 parasitoid species (Hymenoptera and Diptera) was recorded from the sampled herbivores, with 48 species from those on R. reticulatum and 50 species from those on R. macrosepalum. In total, 36 herbivore species were parasitised by 1–18 parasitoid species per host species, although the number of parasitoid species was strongly affected by sample size. Parasitoids that had two or more host species frequently attacked herbivore species from different families or on different host plants, whereas they did not attack species from different herbivore guilds; no parasitoids were shared between external feeders and rollers. Therefore, my results support the hypothesis that few parasitoids are shared among herbivores of different feeding guilds.     

Mathematical theory for plant—herbivore systems

The interactions of host plants with herbivores can be mediated by factors other than population sizes or biomass alone. Recent evidence indicates that features of the vegetation (loosely termed plant quality) may change in response to herbivory and may, in turn, influence the performance of herbivores (i.e. by affecting survivorship, fecundity, or growth rates). A model which incorporates the effect of plant quality is presented. First it is shown that the frequency distribution of plant quality in the vegetation (p(q, t)) satisfies an equation of conservation. Then, qualitative aspects of the system are discussed in three situations: (1) mobile herbivores interacting with all plants; (2) sessile herbivores feeding exclusively on single plants; (3) intermediate situations in which mobility is moderate to low.I show that depending on the plant quality response, f(q, h), and the herbivore response, g(q, h), it is possible to obtain stable equilibria as well as stable periodic oscillations. In the former case the populations tend to lose their heterogeneity. In the latter case, oscillations are accompanied by alternate narrowing and broadening of the distribution. Empirical testing and further research are suggested.     

Species-specific herbivore–herbivore interactions and plant responses to sequential attack by multiple herbivores on a perennial woody plant

When plants are sequentially attacked by multiple herbivores, herbivore identity and host specialization can greatly influence the patterns of herbivore–herbivore and plant–herbivore interactions. However, how prior herbivory and the resulting induced plant responses potentially affect subsequent herbivores deserves further investigation. In this study, we conducted a common-garden experiment that manipulated sequential herbivory by the specialist caterpillar Gadirtha fusca Pogue (Lepidoptera: Nolidae) and the generalist caterpillar Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) on Chinese tallow, Triadica sebifera (L.) Small (Euphorbiaceae). We tested how prior exposure to herbivores with different levels of host specialization affected the performance of subsequently arriving con- and heterospecifics, as well as plant growth and defense responses under subsequent herbivory. We found that prior exposure to the specialist G. fusca facilitated the performance of subsequent conspecifics, resulting in a significant decrease in the growth (height and stem diameter at ground level) of tallow plants. However, prior exposure to the generalist S. litura did not affect the feeding of subsequent con- or heterospecifics or the growth of tallow plants. Sequential herbivory by specialist and generalist conspecifics resulted in lower levels of tannins and flavonoids, respectively, in leaves of tallow plants, whereas sequential herbivory by the two species did not affect the levels of tannins or flavonoids, compared to a single damage event. We conclude that herbivore species-specific plant responses appear to be more important than herbivore identity or specialization in determining herbivore–herbivore interactions and plant responses to sequential herbivore attack.     

Wetland macrophyte diversity, trophic status and phytoplankton： a case study of the cascading effects of an invasive herbivore

Shallow water bodies can exist in alternative stable states, a clear water state with high coverage of macrophytes or a turbid state with high phytoplankton biomass. The alternative equilibria hypothesis has been proposed to explain the occurrence of the alternative stable states (Scheffer et al., 1993)[1], which assumes that: 1),     

δ13C values of an herbivore and the ratio of C3 to C4 plant carbon in its diet

Summary The ¹³C values of whole body samples of the beetle Tribolium castaneum are closely correlated with the ¹³C values of the plant carbon in its diet. The correlation is always high for diets ranging from 100% C₄ to 100% C₃ plant material. The degree of correlation is independent of the growth rate of the animals.     

The ontogenetic stoichiometric bottleneck stabilizes herbivore–autotroph dynamics

In the ecological stoichiometry theory of population dynamics, ontogenetic changes in nutrient demand have been ignored. Here, I studied a stage-structured Daphnia–algae herbivore–autotroph model, in which the juveniles of the herbivore had a higher nutrient (phosphorous) demand for maturation than the adults for reproduction. The model predicted that while an increase in the juvenile nutrient demand (i.e., ontogenetic stoichiometric bottleneck) affects stage-specific performances in complex ways through nutrient dynamics and resource quality, in general it has stabilizing effects on the population dynamics.     

Insect endosymbionts: manipulators of insect herbivore trophic interactions?

Throughout their evolutionary history, insects have formed multiple relationships with bacteria. Although many of these bacteria are pathogenic, with deleterious effects on the fitness of infected insects, there are also numerous examples of symbiotic bacteria that are harmless or even beneficial to their insect host. Symbiotic bacteria that form obligate or facultative associations with insects and that are located intracellularly in the host insect are known as endosymbionts. Endosymbiosis can be a strong driving force for evolution when the acquisition and maintenance of a microorganism by the insect host results in the formation of novel structures or changes in physiology and metabolism. The complex evolutionary dynamics of vertically transmitted symbiotic bacteria have led to distinctive symbiont genome characteristics that have profound effects on the phenotype of the host insect. Symbiotic bacteria are key players in insect–plant interactions influencing many aspects of insect ecology and playing a key role in shaping the diversification of many insect groups. In this review, we discuss the role of endosymbionts in manipulating insect herbivore trophic interactions focussing on their impact on plant utilisation patterns and parasitoid biology.     

Do assortative mating and immigrant inviability help maintain population genetic structuring of an herbivore on a crop and a wild relative?

Population genetic structuring is common among herbivorous insects and frequently is associated with divergent host plants, such as crops and their wild relatives. Previous studies showed population genetic structuring in corn leafhopper Dulbulus maidis in Mexico, such that the species consists of two sympatric, host plant-associated populations: an abundant and widespread "pestiferous” population on maize (Zea mays mays), and a small and localized "wild" population on perennial teosinte (Zea diploperennis). a maize wild relative with a limited distribution. This study addressed whether assortative mating and immigrant inviability mediate genetic structuring of corn leafliopper by comparing the mating and reproductive successes of pestiferous and wild females that colonize their nonassociated host plants against the successes of females colonizing their associated host plants. Assortative mating was assessed by comparing mating frequencies and premating and mating times among females of each population on each host plant: immigrant inviability was assessed by comparing, across two generations, the fecundity, survival, development time, sex ratio, and population growth rate among leafhopper populations and host plants. Our results showed that on maize, and compared to resident, pestiferous females, wild females were more likely to mate, and greater proportions of their offspring survived to adult stage and were daughters;consequently, the per-generation population growth rate on maize was greater for immigrant, wild leafhoppers compared to resident, pestiferous leafhoppers. Our results suggested that wild leafhoppers emigrating to maize have a fitness advantage over resident, pestiferous leafhoppers, while immigrant pestiferous and resident wild leafhoppers on teosinte have similar fitnesses.     

Legacy of avian-dominated plant?herbivore systems in New Zealand

Avian herbivores dominated New Zealand?s pre-settlement terrestrial ecosystems to an unparalleled extent, in the absence of a terrestrial mammal fauna. Approximately 50% (88 taxa) of terrestrial bird species consumed plant foliage, shoots, buds and flowers to some degree, but fewer than half these species were major herbivores. Moa (Dinornithiformes) represent the greatest autochthonous radiation of avian herbivores in New Zealand. They were the largest browsers and grazers within both forest and scrubland ecosystems. Diverse waterfowl (Anatidae) and rail (Rallidae) faunas occupied forests, wetlands and grasslands. Parrots (Psittacidae) and wattlebirds (Callaeidae) occupied a range of woody vegetation types, feeding on fruits/seeds and foliage/ fruits/nectar, respectively. Other important herbivores were the kereru (Columbidae), stitchbird (Notiomystidae) and two honeyeaters (Meliphagidae). Cryptic colouration, nocturnal foraging and fossil evidence suggest that avian populations were strongly constrained by predation. With the absence of migratory avian herbivores, plant structural, constitutive defences prevailed, with the unusual ?wire syndrome? representing an adaptation to limit plant offtake by major terrestrial avian browsers. Inducible plant defences are rare, perhaps reflecting longstanding nutrient-limitations in New Zealand ecosystems. Evidence from coprolites suggests moa were important dispersers of now rare, annual, disturbance-tolerant herb species, and their grazing may have maintained diverse prostrate herbs in different vegetation types. The impact of moa on forest structure and composition remains speculative, but many broadleaved woody species would likely have experienced markedly reduced niches in pre-settlement time. Several distinctive avian-mediated vegetation types are proposed: dryland woodlands, diverse turf swards, coastal herb-rich low-forest-scrubland, and conifer-rich forests. Since human settlement (c. 750 yrs ago), c. 50% of endemic avian herbivore species or c. 40% overall have become extinct, including all moa, 60% of waterfowl and 33% of rail species. Numerically, avian herbivore introductions (c. 24 taxa) since European settlement have compensated for extinctions (c. 27 taxa), but the naturalised birds are mostly small, seed-eating species restricted to human-modified landscapes. Several naturalised species (e.g. Canada goose, Branta canadensis; brown quail, Coturnix ypsilophorus) may provide modes and levels of herbivory comparable with extinct species. The original avian and current introduced mammal herbivore regimes were separated by several centuries when New Zealand lacked megaherbivores. This ?herbivory hiatus? complicates comparisons between pre-settlement and current herbivore systems in New Zealand. However, predation, animal mobility, feeding mode, nutrient transfer patterns and soil impacts were different under an avian regime compared with current mammalian herbivore systems. Levels of ecological surrogacy between avifauna and introduced mammals are less evident. Ungulates generally appear to have impacts qualitatively different from those of the extinct moa. Because of New Zealand?s peculiar evolutionary history, avian herbivores will generally favour the persistence of indigenous vegetation, while mammalian herbivores continue to induce population declines of select plant species, change vegetation regeneration patterns, and generally favour the spread and consolidation of introduced plant species with which they share an evolutionary history.     

The effects of a plant defence priming compound, β-aminobutyric acid,on multitrophic interactions with an insect herbivore and a hymenopterous parasitoid

Biocontrol of aphids by natural enemies is utilized in many organic and integrated pest management schemes. β-aminobutyric acid (BABA), a non-protein amino acid, is a plant defence primer that suppresses growth of some insect herbivores when applied as a root drench. This investigation examined how applying BABA to host plants via the roots may impact on a parasitoid wasp of aphids. Female Aphidius ervi (Haliday) did not discriminate against pea aphids (Acyrthosiphon pisum (Harris)) reared on BABA-treated beans (Vicia faba L.) or show any modified responses to volatiles released from BABA-treated plants. BABA reduced the size of emerging wasps, primarily by inhibiting the growth of the host aphid. Metabolomic analysis revealed BABA in both aphids and emergent wasps indicating some potential for direct physiological inhibition to have occurred. Survival of the parasitoids was only reduced at doses of BABA likely to produce phytotoxic effects in many plant species, thus there may be potential to incorporate plant defence primers like BABA into integrated pest management practices. However, the precise mechanisms of BABA-inhibition of insects still require elucidation.     

Effects of elevated ultraviolet-B radiation on a plant–herbivore interaction

Enhanced ultraviolet-B (UV-B) radiation may have multiple effects on both plants and animals and affect plant–herbivore interactions directly and indirectly by inducing changes in host plant quality. In this study, we examined combined effects of UV-B and herbivory on the defence of the mountain birch (Betula pubescens ssp. czerepanovii) and also the effects of enhanced UV-B radiation on a geometrid with an outbreak cycle: the autumnal moth (Epirrita autumnata). We established an experiment mimicking ozone depletion of 30% (a relevant level when simulating ozone depletion above Northern Lapland). Both arctic species responded only slightly to the enhanced level of UV-B radiation, which may indicate that these species are already adapted to a broader range of UV-B radiation. UV-B exposure slightly induced the accumulation of myricetin glycosides but had no significant effect on the contents of quercetin or kaempferol derivatives. Mountain birch seedlings responded more efficiently to herbivory wounding than to enhanced UV-B exposure. Herbivory induced the activities of foliar oxidases that had earlier been shown to impair both feeding and growth of moth larvae. In contrast, the contents of foliar phenolics did not show the same response in different clones, except for a decrease in the contents of tannin precursors. The induction of foliar phenoloxidase activities is a specific defence response of mountain birches against insect herbivory. To conclude, our results do not support the hypothesis that the outbreak cycle of the autumnal moth can be explained by the cycles of solar activity and UV-B.     

Mechanisms of tolerance to herbivore damage:what do we know?

Identifying mechanisms of tolerance to herbivore damage will facilitate attempts to understand the role of tolerance in the evolutionary and ecological dynamics of plants and herbivores. Investigations of the physiological and morphological changes that occur in plants in response to herbivore damage have identified several potential mechanisms of tolerance. However, it is unlikely that all physiological changes that occur following damage are tolerance mechanisms. Few studies have made direct comparisons between the expression of tolerance and the relative expression of putative mechanisms. I briefly review empirical evidence for some of the better-studied potential mechanisms, including increased photosynthetic activity, compensatory growth, utilization of stored reserves, and phenological delays. For each of these mechanisms I discuss reasons why the relationship between tolerance and these characters may be more complicated than it first appears. I conclude by discussing several empirical approaches, including herbivore manipulations, quantitative trait loci (QTL) analysis, and selection experiments, that will further our understanding of tolerance mechanisms. This revised version was published online in July 2006 with corrections to the Cover Date.     

Seedling–herbivore interactions: insights into plant defence and regeneration patterns

Background

Herbivores have the power to shape plant evolutionary trajectories, influence the structure and function of vegetation, devastate entire crops, or halt the spread of invasive weeds, and as a consequence, research into plant–herbivore interactions is pivotal to our understanding of plant ecology and evolution. However, the causes and consequences of seedling herbivory have received remarkably little attention, despite the fact that plants tend to be most susceptible to herbivory during establishment, and this damage can alter community composition and structure.

Scope

In this Viewpoint article we review why herbivory during early plant ontogeny is important and in so doing introduce an Annals of Botany Special Issue that draws together the latest work on the topic. In a synthesis of the existing literature and a collection of new studies, we examine several linked issues. These include the development and expression of seedling defences and patterns of selection by herbivores, and how seedling selection affects plant establishment and community structure. We then examine how disruption of the seedling–herbivore interaction might affect normal patterns of plant community establishment and discuss how an understanding of patterns of seedling herbivory can aid our attempts to restore semi-natural vegetation. We finish by outlining a number of areas where more research is required. These include a need for a deeper consideration of how endogenous and exogenous factors determine investment in seedling defence, particularly for the very youngest plants, and a better understanding of the phylogenetic and biogeographical patterns of seedling defence. There is also much still be to be done on the mechanisms of seedling selection by herbivores, particularly with respect to the possible involvement of volatile cues. These inter-related issues together inform our understanding of how seedling herbivory affects plant regeneration at a time when anthropogenic change is likely to disrupt this long-established, but all-too-often ignored interaction.