Host selection in phytophagous insects: a new explanation for learning in adults

Insect learning can change the preferences an egg laying female displays towards different host plant species. Current hypotheses propose that learning may be advantageous in adult host selection behaviour through improved recognition, accuracy or selectivity in foraging. In this paper, we present a hypothesis for when learning can be advantageous without such improvements in adult host foraging. Specifically, that learning can be an advantageous strategy for egg laying females when larvae must feed on more than one plant in order to complete development, if the fitness of larvae is reduced when they switch to a different host species. Here, larvae benefit from developing on the most abundant host species, which is the most likely choice of host for an adult insect which increases its preference for a host species through learning. The hypothesis is formalised with a mathematical model and we provide evidence from studies on the behavioural ecology of a number of insect species which demonstrate that the assumptions of this hypothesis may frequently be fulfilled in nature. We discuss how multiple mechanisms may convey advantages in insect learning and that benefits to larval development, which have so far been overlooked, should be considered in explanations for the widespread occurrence of learning.

A general model for host plant selection in phytophagous insects

We develop a general theoretical framework for exploring the host plant selection behaviour of herbivorous insects. This model can be used to address a number of questions, including the evolution of specialists, generalists, preference hierarchies, and learning. We use our model to: (i) demonstrate the consequences of the extent to which the reproductive success of a foraging female is limited by the rate at which they find host plants (host limitation) or the number of eggs they carry (egg limitation); (ii) emphasize the different consequences of variation in behaviour before and after landing on (locating) a host (termed pre- and post-alighting, respectively); (iii) show that, in contrast to previous predictions, learning can be favoured in post-alighting behaviour--in particular, individuals can be selected to concentrate oviposition on an abundant low-quality host, whilst ignoring a rare higher-quality host; (iv) emphasize the importance of interactions between mechanisms in favouring specialization or learning.

Does Gamma-aminobutyric acid function as a plant resistance mechanism against phytophagous insect activity? /

Gamma-aminobutyric acid (GAB A) is a ubiquitous non-protein amino acid synthesized via the decarboxylation of L-glutamate in a reaction catalyzed by the cytosolic enzyme L-glutamate decarboxylase (GAD). In animals it functions as an inhibitory neurotransmitter. In plants it accumulates rapidly in response to various stresses, but its function remains unclear. The hypothesis that GABA accumulation in leaf tissue may function as a plant resistance mechanism against phytophagous insect activity was investigated. GABA accumulation in response to mechanical stimulation, mechanical damage and insect activity was demonstrated. In wt tobacco (Nicotiana tabacum cv Samsun), mechanical stimulation or damage caused GABA to accumulate within 2 min from mean levels of 14 to 37 and 1~9 nmol g-l fresh weight (FW), respectively. In the transgenic tobacco strain CaMVGAD27c overexpressing Petunia GAD, the same treatments caused GABA to accumulate from 12 to 59 and 279 nmol g-l FW, respectively. In the transgenic tobacco strain CaMVGADilC 11 overexpressing Petunia GAD lacking an autoinhibitory domain, mechanical stimulation or damage caused GABA to accumulate from 180 to 309 and 630 nmol g-l FW, respectively. Ambulatory activity by tobacco budworm (TBW) larvae (Heliothis virescens) on leaves of CaMVGAD27c tobacco caused GABA to accumulate from 28 to 80 nmol g-l FW within 5 min. Ambulatory and leaf-rolling activity by oblique banded leaf roller (OBLR) larvae (Choristoneura rosaceana cv Harris) on wt soybean leaves (Glycine max cv Harovinton) caused GABA to accumulate from 60 to 1123 nmol g-l FW within 20 min. Increased GABA levels in leaf tissue were shown to affect phytophagous preference in TBW larvae presented with wt and transgenic tobacco leaves. When presented with leaves of Samsun wt and CaMVGAD27c plants, TBW larvae consumed more wt leaf tissue (640 ± 501 S.D. mm2 ) than transgenic leaf tissue (278 ± 338 S.D. mm2 ) nine times out of ten. When presented with leaves of Samsun wt and CaMVGAD~C11 plants, TBW larvae consumed more transgenic leaf tissue (1219 ± 1009 S.D. mm2 ) than wt leaf tissue (28 ± 31 S.D. mm2 ) ten times out of ten. These results indicate that: (1) ambulatory activity of insect larvae on leaves results in increased GABA levels, (2) transgenic tobacco leaves with increased capacity for GABA synthesis deter feeding, and (3) transgenic tobacco leaves with constitutively higher GABA levels stimulate feeding.

Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects.

Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93 PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding, and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are important for the adaptation of plants to pathogenic fungi and phytophagous insects.

Mortality Risk in Insects

Understanding how and why insect numbers fluctuate through time and space has been a central theme in ecological research for more than a century. Life tables have been used to understand temporal and spatial patterns in insect numbers. In this study, we estimated cause-of-death probabilities for phytophagous insects using multiple decrement life tables and the irreplaceable mortality analytic technique. Multiple decrement life tables were created from 73 insect life tables published from 1954 to 2004. Irreplaceable mortality (the portion of mortality that cannot be replaced by another cause) from pathogens, predators, and parasitoids was 8.6 +/- 7.2, 7.8 +/- 4.9, and 6.2 +/- 1.6%, respectively. In contrast, the mean irreplaceable mortality from all non-natural enemy mortality factors (mortality from factors other than natural enemies) was 35.1 +/- 4.4%. Irreplaceable mortality from natural enemies was significantly lower compared with non-natural enemy factors. Our results may partially explain cases of unsuccessful efficacy in classical biological control, after successful establishment, by showing low irreplaceable mortality for natural enemies, including 5.2 +/- 1.6% for introduced natural enemies. We suggest that the environment (i.e., the degree of environmental stability) influences the magnitude of the irreplaceable mortality from natural enemies. Our results lead to several testable hypotheses and emphasize that it is not possible to estimate the effect of any mortality factor without considering its interaction with competing mortality factors, which has far-reaching consequences for population biology and applied ecology.

Biological control of phytophagous arthropods in the physic nut tree Jatropha curcas L. in Brazil

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)

Rapid [Gamma]-amino acid synthesis and the inhibition of the growth and development of oblique banded leaf-roller larvae

The hypothesis that rapid y-aminobutyric acid (GABA) accumulation is a plant defense against phytophagous insects was investigated. Simulation of mechanical damage resulting from phytophagous insect activity increased soybean (Glycine max L.) leaf GABA 10- to 25-fold within 1 to 4 min. Pulverizing leaf tissue resulted in a value of 2. 15 (±O. 11 SE) ~mol GABA per gram fresh weight. Increasing the GABA levels in a synthetic diet from 1.6 to 2.6 Jlffiol GABA per gram fresh weight reduced the growth rates, developmental rates, total biomass (50% reduction), and survival rates (30% reduction) of cultured Oblique banded leaf-roller (OBLR) (Choristonellra rosacealla Harris) larvae. In field experiments OBLR larvae were found predominantly on young terminal leaves which have a reduced capacity to produce GABA in response to mechanical damage. Glutamate decarboxylase (GAD) is a cytosolic enzyme which catalyses the decarboxylation of L-Glu to GABA. GAD is a calmodulin binding enzyme whose activity is stimulated dramatically by increased cytosolic H+ or Ca2 + ion concentrations. Phytophagous insect activity will disrupt the cellular compartmentation of H+ and Ca2 +, activate GAD and subsequent GABA accumulation. In animals GABA is a major inhibitory neurotransmitter. The possible mechanisms resulting in GABA inhibited growth and development of insects are discussed.

The roles of olfaction and vision in host-plant finding by the diamondback moth, Plutella xylostella

The relative roles of olfaction and vision in the crepuscular host-finding process of a major lepidopteran pest of cruciferous crops, the diamondback moth Plutella xylostella are investigated in a series of laboratory and semi-field experiments. Flying female moths use volatile plant chemical cues to locate and to promote landing on their host, even in complex mixed-crop environments in large cages. Multiple regression analysis shows that both the plant position (front, middle or back rows) and the type of plant (host plant, nonhost plant) are needed to explain the distribution of insects in such a mixed-crop situation. This strong plant position effect indicates that, when host plants are present in a mixture, foraging P. xylostella are more likely to alight on the first row of the plants. The findings are discussed with regard to current theories of host-plant location by phytophagous insects and the possible implications for integrated pest management.

The role of weeds in supporting biological diversity within crop fields

Weeds are major constraints on crop production, yet as part of the primary producers within farming systems, they may be important components of the agroecosystem. Using published literature, the role of weeds in arable systems for other above-ground trophic levels are examined. In the UK, there is evidence that weed flora have changed over the past century, with some species declining in abundance, whereas others have increased. There is also some evidence for a decline in the size of arable weed seedbanks. Some of these changes reflect improved agricultural efficiency, changes to more winter-sown crops in arable rotations and the use of more broad-spectrum herbicide combinations. Interrogation of a database of records of phytophagous insects associated with plant species in the UK reveals that many arable weed species support a high diversity of insect species. Reductions in abundances of host plants may affect associated insects and other taxa. A number of insect groups and farmland birds have shown marked population declines over the past 30 years. Correlational studies indicate that many of these declines are associated with changes in agricultural practices. Certainly reductions in food availability in winter and for nestling birds in spring are implicated in the declines of several bird species, notably the grey partridge, Perdix perdix . Thus weeds have a role within agroecosystems in supporting biodiversity more generally. An understanding of weed competitivity and the importance of weeds for insects and birds may allow the identification of the most important weed species. This may form the first step in balancing the needs for weed control with the requirements for biodiversity and more sustainable production methods.

An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale co-phylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on average, wasps had sequences from 77% of six genes (5.6kb), figs had sequences from 60% of five genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based co-phylogenetic analyses further support the co-diversification hypothesis. Biogeographic analyses indicate that the presentday distribution of fig and pollinator lineages is consistent with an Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term co-diversification.

Contrasting effects of necrotrophic and biotrophic plant pathogens on the aphid Aphis fabae

Phytophagous insects have to contend with a wide variation in food quality brought about by a variety of factors intrinsic and extrinsic to the plant. One of the most important factors is infection by plant pathogenic fungi. Necrotrophic and biotrophic plant pathogenic fungi may have contrasting effects on insect herbivores due to their different infection mechanisms and induction of different resistance pathways, although this has been little studied and there has been no study of their combined effect. We studied the effect of the biotrophic rust fungus Uromyces viciae-fabae (Pers.) Schroet (Basidiomycota: Uredinales: Pucciniaceae) and the necrotrophic fungus Botrytis cinerea Pers. (Ascomycota: Helotiales: Sclerotiniaceae) singly and together on the performance of the aphid Aphis fabae Scop. (Hemiptera: Aphididae) on Vicia faba (L.) (Fabaceae). Alone, botrytis had an inhibitory effect on individual A. fabae development, survival and fecundity, while rust infection consistently enhanced individual aphids’ performance. These effects varied in linear relation to lesion or pustule density. However, whole-plant infection by either pathogen resulted in a smaller aphid population of smaller aphids than on uninfected plants, indicating a lowering of aphid carrying capacity with infection. When both fungi were applied simultaneously to a leaf they generally cancelled the effect of each other out, resulting in most performance parameters being similar to the controls, although fecundity was reduced. However, sequential plant infection (pathogens applied five days apart) led to a 70% decrease in fecundity and 50% reduction in intrinsic rate of increase. The application of rust before botrytis had a greater inhibitory effect on aphids than applying botrytis before rust. Rust infection increased leaf total nitrogen concentration by 30% while infection by botrytis with or without rust led to a 38% decrease. The aphids’ responses to the two plant pathogens individually is consistent with the alteration in plant nutrient content by infection and also the induction of different plant defence pathways and the possible cross-talk between them. This is the first demonstration of the complex effects of the dual infection of a plant by contrasting pathogens on insect herbivores. Key words: Vicia faba, Botrytis cinerea, Uromyces viciae-fabae, tripartite interactions, induced resistance

An exploratory insect survey of tropical soda apple in Brazil and Paraguay

An exploratory survey was conducted in Brazil and Paraguay to record insects feeding on Solanum viarum Dunal (Solanaceae). A list of insects collected is included. The survey indicated that a diverse group of phytophagous insects is associated with S. viarum, and some of them may have potential as biocontrol agents of S. viarum in Florida.

Effect of constituents of the foliar wax of Didymopanax vinosum on the foraging activity of the leaf-cutting ant Atta sexdens rubropilosa

Leaf epicuticular waxes may affect substrate selection by leaf-cutting ants, and host recognition by several phytophagous insects. The influence of the crude epicuticular wax of Didymopanax vinosum E. March. (Araliaceae), and its major constituents lupeol and free primary alcohols, on substrate selection by the leaf-cutting ant Atta sexdens rubropilosa Forel, was investigated. Two ant colonies were used in laboratory bioassays. Corn flakes (zea) were impregnated with chloroform solutions of the substances being tested and fed to the adults. One of the colonies gave results, in most of the tests, not significantly different from the controls. The other colony, however, discriminated against the crude wax, a strong deterrent effect being observed from the first of a series of eight trials. The same colony was able to discriminate against lupeol after the second trial. The fraction of primary n-alcohols (22% C28, 66% C30 and 12% C32) deterred feeding only after the fifth trial. The results demonstrate that some constituents of epicuticular waxes may deter the foraging activity of A. sexdens rubropilosa, depending, however, on the colony under observation. It is suggested that lupeol, of the foliar wax of D. vinosum, is an important deterrent to leaf-cutting ants, although with less pronounced effects than those observed in tests with the crude wax.