Food preference and performance of the larvae of a specialist herbivore: variation among and within host-plant populations

Specialist herbivores are suggested to be unaffected by or attracted to the defense compounds of their host-plants, and can even prefer higher levels of certain chemicals. Abrostola asclepiadis is a specialist herbivore whose larvae feed on the leaves of Vincetoxicum hirundinaria, which contains toxic alkaloids and is unpalatable to most generalist herbivores. The food choice, leaf consumption and growth of A. asclepiadis larvae were studied to determine whether there is variation among and within host-plant populations in their suitability for this specialist herbivore. There was significant variation in food preference and leaf consumption among host-plant populations, but no differences were found in larval growth and feeding on different host-plant populations. A. asclepiadis larvae preferred host-plant populations with higher alkaloid concentrations, but did not consume more leaf material from plants originating from such populations in a no-choice experiment. There was also some variation in food preference of larvae among host-plant individuals belonging to the same population, suggesting that there was variability in leaf chemistry also within populations. Such variation in larval preference among host-plant genotypes and populations may create potential for coevolutionary dynamics in a spatial mosaic.     

Host-plant genotype and other herbivores influence goldenrod stem galler preference and performance

Ecologists have labored to find an explanation for the lack of a positive correlation between host preference and offspring performance in herbivorous insects. This study focuses on how one herbivore species can influence another herbivore species’ ability to accurately assess the suitability of different host-plant genotypes for larval development. In particular, we examined the role that an early season xylem-feeding homopteran (meadow spittlebug, Philaenus spumarius) has on the preference-performance correlation of a late-season dipteran stem galler (Eurosta solidaginis) among different goldenrod genotypes. In a greenhouse, we released adult stem gallers into replicate cages that contained ramets from four different goldenrod genotypes crossed with three densities of spittlebugs (0, 1, or 8 nymphs placed 2 weeks previously on each ramet). Spittlebug feeding caused a density-dependent decline in ramet growth rates, which in turn caused a corresponding decrease in host-plant preference by the stem gallers (number of ovipunctures per bud or proportion of ramets attacked). Goldenrod genotype and the interaction between spittlebugs and genotypes also influenced host-plant preference by the stem galler. Goldenrod genotype had the greatest impact on stem galler offspring performance (gall size or survivorship). Spittlebug density also affected performance, but only through its interaction with goldenrod genotype. On some genotypes, the survivorship of stem-galler larvae decreased with increasing spittlebug density, while on other genotypes, survivorship remained unchanged, or actually increased, with increasing spittlebug density. This suggests that there was genetic variance among goldenrod genotypes in their norms of reaction for their suitability as a host to the stem gallers. One possible explanation for why spittlebugs caused a significant reduction in preference, but not in performance, was that spittlebugs had very few long-term effects on the host plant. Flower number, flowering phenology, and the allocation of the ramet’s biomass to different structures (below-ground organs, stems, leaves, and flowers) were unchanged with respect to spittlebug density. The only effect of spittlebugs was a 3–4% decrease in ramet height at the end of the growing season. We argue that the lack of a positive correlation between host-plant preference and larval performance may reflect a constraint on the discriminatory ability of female stem gallers. The damage to goldenrods caused by spittlebugs prior to attack by the stem gallers is similar in effect to potentially innumerable other causes of goldenrod stress (e.g., reduction in ramet growth rates). As a consequence, stem gallers may not be able to discern the subtle differences among stresses that identify those that will negatively affect the fitness of stem-galler offspring. The fact that goldenrod genotypes differ in their response to stresses would only further complicate the host-selection process. We propose that the stem gallers may have evolved a strategy that uses simple cues as the basis for rejecting similarly stressed plants, whether all of those plant genotype-stress combinations reduce performance or not. Received: 26 January 1999 / Accepted: 2 June 1999     

Extinction-colonization dynamics and host-plant choice in butterfly metapopulations

Species living in highly fragmented landscapes often occur as metapopulations with frequent population turnover. Turnover rate is known to depend on ecological factors, such as population size and connectivity, but it may also be influenced by the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly (Melitaea cinxia) in Finland uses two host-plant species that vary in their relative abundances among distinct habitat patches (dry meadows) in a large network of approximately 1,700 patches. We found no effect of host species use on local extinction. In contrast, population establishment was strongly influenced by the match between the host species composition of an empty habitat patch and the relative host use by larvae in previous years in the habitat patches that were well connected to the target patch. This "colonization effect" could be due to spatially variable plant acceptability or resistance or to spatially variable insect oviposition preference or larval performance. We show that spatial variation in adult oviposition preference occurs at the relevant spatial scale and that the other possible causes of the colonization effect can be discounted. We conclude that the colonization effect is generated by host preference influencing the movement patterns of ovipositing females. Migrant females with dissimilar host preferences have different perceptions of relative patch quality, which influences their likelihood of colonizing patches with particular host composition.     

Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore

Summary Plant resistance to insect herbivores may derive from traits influencing herbivore preference, traits influencing the suitability of the plant as a host, or both. However, the plant traits influencing host-plant selection by ovipositing insect herbivores may not completely overlap those traits that affect larval survival, and distinct traits may exhibit different levels of genetic vs. environmental control. Therefore, resource supply to the host plant could affect oviposition preference and larval performance differently in different plant genotypes. To test this hypothesis, the effects of resistance level, plant genotype, and resource supply to the host plant on oviposition preference and larval performance of a gallmaking herbivore, and on various plant traits that could influence these, were examined. Replicates of four genotypes of Solidago altissima, grown under low, medium, or high levels of nutrient supply in full sun or with medium levels of nutrients in shade, were exposed to mass-released Eurosta solidaginis. The number of plants ovipunctured was significantly affected by plant genotype and the interaction between genotype and nutrient supply to the host plant: one susceptible and one resistant genotype were more preferred, and preference tended to increase with nutrient supply in the more-preferred genotypes. The growth rate of ovipunctured plants during the oviposition period was significantly greater than that of unpunctured plants. Bud diameter (which was strongly correlated with plant growth rate), leaf area, and leaf water content were significant determinants of the percentage of plants ovipunctured, explaining 74% of the variance. The number of surviving larvae was significantly affected by plant genotype, but no effect of nutrient or light supply to the host plant was detected. The ratio of bud diameter to bud length was positively related to the percentage of ovipunctured plants that formed galls, suggesting that the accurate placement of eggs near the apical meristem by ovipositing females may be easier in short, thick buds. No significant correlation was observed between oviposition preference and larval survival at the population level. These results suggest that the plant traits affecting oviposition preference may exhibit different magnitudes of phenotypic plasticity than those affecting larval survival, and that the degree of phenotypic plasticity in plant traits affecting oviposition preference may differ among genotypes within a species.     

The ‘mother knows best’ principle: should soil insects be included in the preference–performance debate?

Abstract.  1. Few entomological studies include soil-dwelling insects in mainstream ecological theory, for example the preference–performance debate. The preference–performance hypothesis predicts that when insect herbivores have offspring with limited capacity to relocate in relation to a host plant, there is a strong selection pressure for the adult to oviposit on plants that will maximise offspring performance.
2. This paper discusses the proposition that insect herbivores that live above ground, but have soil-dwelling offspring, should be included in the preference–performance debate. Twelve relevant studies were reviewed to assess the potential for including soil insects in this framework, before presenting a preliminary case study using the clover root weevil ( Sitona lepidus ) and its host plant, white clover ( Trifolium repens ).
3. Maternal S. lepidus preferentially oviposited on T. repens plants that had rhizobial root nodules (which enhance offspring performance) rather than T. repens plants without nodules, despite plants having similar foliar nutritional quality. This suggests that adult behaviour above ground was influenced by below-ground host-plant quality.
4. A conceptual model is presented to describe how information about the suitability for offspring below ground could underpin oviposition behaviour of parental insects living above ground, via plant- and soil-mediated semiochemicals. These interactions between genetically related, but spatially separated, insect herbivores raise important evolutionary questions such as how induced plant responses above ground affect offspring living below ground and vice versa.     

GENETIC COVARIANCE BETWEEN OVIPOSITION PREFERENCE AND LARVAL PERFORMANCE IN AN INSECT HERBIVORE

An experimental study determined that females of the herbivorous fly species Liriomyza sativae (Diptera: Agromyzidae) preferentially oviposit on the plant species on which their female progeny attain the greatest pupal weight. A modified parent/offspring regression was used to quantify this relationship as an additive genetic covariance between host-plant preference and relative performance of female larvae on different plant species. The implications of a genetic covariance between preference and performance on the course of evolution in herbivores are discussed. Several females from one population refused to oviposit on one of the plant species; this population also suffered the only significant larval mortality on this plant. These results corroborate the avoidance of unsuitable host plants seen in the genetic analyses of individuals, but relative to the genetic data, such population-level data are of limited usefulness in the study of evolutionary mechanisms by which insect populations become adapted to their host plants.     

How foraging tactics determine host-plant use by a polyphagous caterpillar

The use of multiple host-plant species by populations of insect herbivores can result from a variety of possible ecological and behavioral mechanisms. An understanding of the foraging mechanisms determining polyphagy in relation to local ecological conditions is therefore essential to understanding the evolutionary ecology of polyphagy. Here, we evaluate patterns of host-plant use by the polyphagous caterpillar Grammia geneura (Lepidoptera: Arctiidae) in relation to host-plant availability and foraging tactics of individuals. Field surveys of caterpillar feeding and plant abundance carried out across several sites, seasons, and years showed that: (1) G. geneura consistently preferred forbs to grasses and woody plants, (2) forb-feeding was opportunistic, supporting the idea that caterpillars sample locally available host-plants, and (3) there were consistent patterns of host-plant use that were not explained by host-plant availability (electivity). An independent set of 7-h observations of 11 caterpillars showed that electivity for a subset of caterpillar-host associations could be explained by variation in the probability of initiating feeding and the average duration of feeding bouts on different hosts but not by variation in the probability of encountering different hosts, thus providing a behavioral basis for the observed variation in host-plant use. The use of detailed foraging tactics by larvae to explain host-plant use at the population level is a novel contribution of this study.     

Host plant genotype influences survival of hybrids between Eurosta solidaginis host races

Extrinsic, host-associated environmental factors may influence postmating isolation between herbivorous insect populations and represent a fundamentally ecological cause of speciation. We investigated this issue in experiments on hybrids between the host races of Eurosta solidaginis, a fly that induces galls on the goldenrods Solidago altissima and S. gigantea. To do so, we measured the performance of parental host races and their hybrids on five genotypes of S. gigantea and nine genotypes of S. altissima to test hypotheses about how variation in plant genotype affects performance (i.e., fitness) and potentially influences gene flow between these host races. We found that rates of gall induction and of survival to adult emergence by hybrid larvae were significantly lower than those of both parental host races on both host species, adding support to the hypothesis that there is partial postmating isolation between the host races. Hybrid flies significantly varied in their performance across plant genotypes of both host species. A significant interaction between the effects of plant genotype and mating treatment (parental vs. hybrid crosses) on larval performance indicated that the relative suitability of particular plant genotypes differed between the parental host races and their hybrids. These patterns illustrate a poor correspondence between optimal parental and hybrid environments, consistent with the hypothesis that these host races are partially isolated due to extrinsic (ecological) factors. Based on these findings, we discuss the possibility that plant genotypes in which hybrid performance is high can facilitate hybridization and gene flow between partially reproductively isolated populations of herbivorous insects, thus affecting the dynamics of ecological speciation.     

Temporal dynamics in non-additive responses of arthropods to host-plant genotypic diversity

Genotypic diversity within host‐plant populations has been linked to the diversity of associated arthropod communities, but the temporal dynamics of this relationship, along with the underlying mechanisms, are not well understood. In this study, we employed a common garden experiment that manipulated the number of genotypes within patches of Solidago altissima, tall goldenrod, to contain 1, 3, 6 or 12 genotypes m^?2 and measured both host‐plant and arthropod responses to genotypic diversity throughout an entire growing season. Despite substantial phenological changes in host plants and in the composition of the arthropod community, we detected consistent positive responses of arthropod diversity to host‐plant genotypic diversity throughout all but the end of the growing season. Arthropod richness and abundance increased with genotypic diversity by up to～65%. Furthermore, arthropod responses were non‐additive for most of the growing season, with up to 52% more species occurring in mixtures than the number predicted by summing the number of arthropods associated with component genotypes in monoculture. Non‐additive arthropod responses were likely driven by concurrent non‐additive increases in host‐plant aboveground biomass. Qualitative differences among host‐plant genotypes were also important early in the season, when specialist herbivores dominated the arthropod community. Neither arthropod diversity nor flower number was associated with genotypic diversity at the end of the growing season, when generalist floral‐associated herbivores dominated. Taken together, these results show that focusing on the temporal dynamics in the quantity and quality of co‐occurring host‐plant genotypes and associated community composition can help uncover the mechanisms that link intraspecific host‐plant diversity to the structure of arthropod communities. Furthermore, consistent non‐additive effects in genotypically diverse plots may limit the predictability of the arthropod community based solely on the genetic make‐up of a host‐plant patch.     

Individual variation in two host plants of the ladybird beetle,Epilachna pustulosa (Coleoptera: Coccinellidae)

Individual variation in two species of host plants (thistle,Cirsium kamtschaticum, and blue cohosh,Caulophyllum robustum) of the herbivorous ladybird beetleEpilachna pustulosa was examined under laboratory conditions for their acceptability to adult beetles as a food resource, for adult preference and for larval performance. When clones of these plants were subjected to non-choice tests using posthibernating female beetles, there was found to be significant intraspecific variation among clones in terms of their acceptability, but interspecific variation was not detected. Significant intraspecific as well as interspecific variation were frequently detected in the two host plants when clones of these plants were subjected to choice tests using posthibernating female beetles; the magnitude of interspecific plant variation for beetle preference is not necessarily larger than that of intraspecific plant variation. Individual variation across plant species with respect to beetle larval performance was also significant. A positive correlation between adult preference and larval performance is suggested across the two taxonomically remote host plant species, thistle and blue cohosh, although this needs further investigation.     

Relationship between oviposition preference and offspring performance in Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Abstract We investigated the oviposition preference and larval performance of Helicoverpa armigera under laboratory conditions to determine if the oviposition preference of individual females on maize, cowpea and cotton correlates with offspring performance on the leaves of the same host plants. The host-plant preference hierarchy of females did not correlate with their offspring performance. Female moths chose host plants that contributed less to their offspring fitness. Plant effects accounted for the largest amount of variation in offspring performance, while the effects of female (family) was low. The offspring of most females (80%, n  = 10) were broadly similar, but 20% (two out of 10), showed marked difference in their offspring performance across the host-plant species. Similarly, there was no relation between larval feeding preference and performance. However, like most laboratory experiments, our experi-mental design does not allow the evaluation of ecological factors (for example, natural enemies, host abundance, etc.) that can play an important role in larval performance in the field. Overall, the results highlight the importance of carrying out preference performance analysis on the individual or family level, rather than pooling individuals to obtain average population data.     

Quantitative genetics of preference and performance on chickpeas in the noctuid moth, Helicoverpa armigera

If a novel, resistant host-plant genotype arises in the environment, insect populations utilising that host must be able to overcome that resistance in order that they can maintain their ability to feed on that host. The ability to evolve resistance to host-plant defences depends upon additive genetic variation in larval performance and adult host-choice preference. To investigate the potential of a generalist herbivore to respond to a novel resistant host, we estimated the heritability of larval performance in the noctuid moth, Helicoverpa armigera, on a resistant and a susceptible variety of the chickpea, Cicer arietinum, at two different life stages. Heritability estimates were higher for neonates than for third-instar larvae, suggesting that their ability to establish on plants could be key to the evolution of resistance in this species; however, further information regarding the nature of selection in the field would be required to confirm this prediction. There was no genetic correlation between larval performance and oviposition preference, indicating that female moths do not choose the most suitable plant for their offspring. We also found significant genotype by environment interactions for neonates (but not third-instar larvae), suggesting that the larval response to different plant genotypes is stage-specific in this species.     

Mitochondrial DNA variation among host races of Eurosta solidaginis Fitch (Diptera: Tephritidae)

Eurosta solidaginis Fitch (Diptera: Tephritidae) induces galls on two species of goldenrod, Solidago (Compositae), in the northern regions of the United States. Recent studies have demonstrated that E. solidaginis is comprised of two host races that differ in adult emergence times, mate preference, and host preference. However, it is not known how much genetic variation, if any, exists among E. solidaginis host-associated populations west of Minnesota where the two host races occur in sympatry. Sequencing analysis was used to characterize two mitochondrial gene fragments: (1) NADH1 dehydrogenase (ND1: 539 bp) and (2) cytochrome oxidase II + tRNA(Lys) + tRNA(Asp) (CO2KD: 396 bp) from sympatric, host-associated populations of E. solidaginis in North Dakota. Our results indicated that two genetically distinct lineages exist among E. solidaginis in North Dakota that correspond with host-plant association.     

Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective

Most herbivorous arthropods are specialists that feed on one or a few related plant species. To understand why this is so, both mechanistic and functional studies have been carried out, predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of secondary plant chemicals as source of information in behavioural decisions of herbivores. Many evolutionary studies have regarded co-evolution between plants and herbivores to explain the diversity of secondary plant chemicals and host specialisation of herbivores. However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of fitness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69, 886-892)] has initiated a discussion on the need of a multitrophic perspective to understand the evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly resulted in ecological studies on host-selection behaviour that take a multitrophic perspective. Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies and competitors can affect herbivore behaviour. These cues may constitute important information on fitness prospects, just as plant cues can do. In this paper I selectively review how information from organisms at different trophic levels varies in space and time and how herbivores can integratively exploit this information during host selection. In doing so, research areas are identified that are likely to provide important new insights to explain several of the questions in herbivore host selection that remain unanswered so far. These research areas are at the interface of evolutionary ecology, behavioural ecology and chemical ecology.     

Host-plant susceptibility to the carrot fly, Psila rosae. 3. The role of oviposition preferences and larval performance

The acceptability of various plant species to ovipositing carrot flies was weakly, but significantly correlated with the host's suitability for larval development. Both adult host-plant preferences and larval performance as determined in laboratory experiments explained a part of the variation in susceptibility among the various test plants observed in the field. Across the whole set of plant species examined, antixenosis contributed more substantially to resistance than antibiosis, while the reverse seemed to be true for carrot cultivars.     

Optimization of adult performance determines host choice in a grass miner.

Models and empirical studies on host selection in plant-insect, algae-amphipod, host-parasite and prey-predator systems assume that oviposition preference is determined by the quality of the oviposition site for offspring development. According to the oviposition-preference-offspring-performance hypothesis, oviposition-preference hierarchy should correspond to host suitability for offspring development because females maximize their fitness by optimizing offspring performance. We show, we believe for the first time, that adult feeding site and related adult performance may explain most of the variation in adult feeding and oviposition site selection of an oligophagous grass miner, Chromatomyia nigra (Diptera). This study advances our understanding of the complex interactions between plants and herbivores because it shows that host-preference patterns are not only shaped by the optimization of offspring performance, as previously assumed, but also by the optimization of adult performance.     

Host preference of plant genotypes is altered by intraspecific competition in a phytophagous insect

Variation among aphid genotypes leads them to preferentially colonize different host-plant genotypes. In a natural community, different genotypes within a species are expected to coexist on a single host plant, and these aphids can interact, potentially, altering host-plant preferences. Using a model aphid (Sitobion avenae) and barley (Hordeum vulgare) system, we compared aphid preference and performance in one- or two-genotype colonies in pots with genetically diverse host plants (6 genotypes) or genetically uniform host plants (1 genotype per pot). Aphid host preference was shown to differ when a second aphid genotype was present, with one aphid genotype exhibiting a preference change due to the genotypic identity of the second aphid. The population growth rate of the aphids was not influenced by the competitor, and thus, we conclude that these effects are due to aphid distribution (preference) rather than effects through performance. Our work demonstrates that within a complex ecological community, an individual’s behavior can be influenced by interactions with other genotypes within the same species, as well as interactions with genotypes of other species.     

Unique arthropod communities on different host-plant genotypes results in greater arthropod diversity

Studies on the effect of plant-species diversity on various ecological processes has led to the study of the effects of plant-genetic diversity in the context of community genetics. Arthropod diversity can increase with plant-species or plant-genetic diversity (Wimp et al. in Ecol Lett 7:776–780, 2004). Plant diversity effects can be difficult to separate from other ecological processes, for example, complementarity. We asked three basic questions: (1) Are arthropod communities unique on different host-plant genotypes? (2) Is arthropod diversity greater when associated with greater plant-genetic diversity? (3) Are arthropod communities more closely associated with host-plant genetics than the plant neighborhood? We studied canopy arthropods on Populus fremontii trees randomly planted in a common garden. All trees were planted in a homogeneous matrix, which helped to reduce P. fremontii neighborhood effects. One sample was comprised of few P. fremontii genotypes with many clones. A second sample was comprised of many P. fremontii genotypes with few clones. A second data set was used to examine the relationships between the arthropod community with P. fremontii genetic composition and the neighborhood composition of the focal host plant. Unique arthropod communities were associated with different P. fremontii genotypes, and arthropod community diversity was greater in the sample with greater P. fremontii genotypic diversity. Arthropod community similarity was negatively correlated with P. fremontii genetic distance, but arthropod community similarity was not related to the neighborhood of the P. fremontii host plant.     

Does host plant quality affect the oviposition decisions of an omnivore?

Optimal oviposition theory predicts a positive relationship between female preference for oviposition hosts and offspring performance. Interspecies effects on oviposition preference have been widely investigated, especially for herbivores. However, intraspecies variation, such as nitrogen content, might also influence female preference for oviposition hosts and subsequent offspring performance. To evaluate this possibility, we investigated the oviposition preference of a zoophytophagous omnivore and the development and survival of its nymphs on a single species of host plant that varied in nitrogen content. In choice and no‐choice experiments without prey, female omnivores were allowed to oviposit on plants that had been fertilized using 4 rates of nitrogen fertilizer (39, 78, 156, and 311 mg/L nitrogen) for 72 h. After 72 h, the most females were found on tomato plants receiving high concentrations of nitrogen fertilizer and more eggs were laid on those plants. First instar nymphs developed more rapidly on high‐nitrogen plants and third instar nymphs developed faster on low‐nitrogen plants. Plant nitrogen did not affect nymph survival to the adult stage, or the probability of survival over time. Although female omnivores did discriminate between potential oviposition hosts based on plant nitrogen, their choices did not significantly impact nymph development or survival. This is the first study to show that intraspecies variation in nitrogen content between plants affects the oviposition preference of female omnivores, but not offspring performance.     

Dispersal ability and host-plant characteristics influence spatial population structure of monophagous beetles

Abstract.  1. Dispersal plays an integral role in determining spatial population structure and, consequently, the long-term survival of many species. Theoretical studies indicate that dispersal increases with population density and decreasing habitat stability. In the case of monophagous insect herbivores, the stability of host-plant populations may influence their spatial population structure.
2. The tallgrass prairie in Iowa, U.S.A. is highly fragmented and most prairie insects face a landscape with fewer habitat patches and smaller host-plant populations than 150 years ago, potentially making dispersal between patches difficult. Some herbivores, however, use native plant species with weedy characteristics that have increased in abundance because of disturbances.
3. Mark–recapture data and presence–absence surveys were used to examine dispersal and spatial population structure of two monophagous beetles with host plants that exhibit different population stability and have responded differently to fragmentation of tallgrass prairie.
4. Chrysochus auratus Fabricius exhibits a patchy population structure and has relatively large dispersal distances and frequencies. Its host plant is variable locally in time and space, but is more abundant than 150 years ago. The other species, Anomoea laticlavia Forster, exhibits a metapopulation or non-equilibrium population structure and has relatively small dispersal distances and frequencies. Its host-plant populations are stable in time and space.
5. The results indicate that dispersal ability of monophagous beetles reflects the life-history dynamics of their host plants, but the spatial population structure exhibited today is strongly influenced by how the host plants have responded to the fragmentation process over both time and space.