John Paul Cunningham

Learning in Helicoverpa armigera (Lepidoptera: Noctuidae): a new look at the behaviour and control of a polyphagous pest

Recent experimental evidence has shown that learning occurs in the host selection behaviour of Helicoverpa armigera (Hubner), one of the world‘s most important agricultural pests. This paper discusses how the occurrence of learning changes our understanding of the host selection behaviour of this polyphagous moth. Host preferences determined from previous laboratory studies may be vastly different from preferences exhibited by moths in the field, where the abundance of particular hosts may be more likely to determine host preference. In support of this prediction, a number of field studies have shown that the ‘attractiveness’ of different hosts for H. armigera oviposition may depend on the relative abundance of these host species. Insect learning may play a fundamental role in the design and application of present and future integrated pest management strategies such as the use of host volatiles, trap crops and resistant crop varieties for monitoring and controlling this important pest species.

Understanding Heliothine (Lepidoptera: Heliothinae) Pests: What is a Host Plant?

ABSTRACT Heliothine moths (Lepidoptera: Heliothinae) include some of the worlds most devastating pest species. Whereas the majority of nonpest heliothinae specialize on a single plant family, genus, or species, pest species are highly polyphagous, with populations often escalating in size as they move from one crop species to another. Here, we examine the current literature on heliothine host-selection behavior with the aim of providing a knowledge base for research scientists and pest managers. We review the host relations of pest heliothines, with a particular focus on Helicoverpa armigera (Hübner), the most economically damaging of all heliothine species. We then consider the important question of what constitutes a host plant in these moths, and some of the problems that arise when trying to determine host plant status from empirical studies on host use. The top six host plant families in the two main Australian pest species (H. armigera and Helicoverpa punctigera Wallengren) are the same and the top three (Asteraceae, Fabaceae, and Malvaceae) are ranked the same (in terms of the number of host species on which eggs or larvae have been identified), suggesting that these species may use similar cues to identify their hosts. In contrast, for the two key pest heliothines in the Americas, the Fabaceae contains ≈1/3 of hosts for both. For Helicoverpa zea (Boddie), the remaining hosts are more evenly distributed, with Solanaceae next, followed by Poaceae, Asteraceae, Malvaceae, and Rosaceae. For Heliothis virescens (F.), the next highest five families are Malvaceae, Asteraceae, Solanaceae, Convolvulaceae, and Scrophulariaceae. Again there is considerable overlap in host use at generic and even species level. H. armigera is the most widely distributed and recorded from 68 plant families worldwide, but only 14 families are recorded as a containing a host in all geographic areas. A few crop hosts are used throughout the range as expected, but in some cases there are anomalies, perhaps because host plant relation studies are not comparable. Studies on the attraction of heliothines to plant odors are examined in the context of our current understanding of insect olfaction, with the aim of better understanding the connection between odor perception and host choice. Finally, we discuss research into sustainable management of pest heliothines using knowledge of heliothine behavior and ecology. A coordinated international research effort is needed to advance our knowledge on host relations in widely distributed polyphagous species instead of the localized, piecemeal approaches to understanding these insects that has been the norm to date.

Learning in the nectar foraging behaviour of Helicoverpa armigera

Abstract.1. Learning may enable insects to obtain nectar from flowers more efficiently. Learning in nectar foraging has been shown primarily in studies of bees and butterflies. Here, learning is demonstrated in the nectar foraging behaviour of a noctuid moth, Helicoverpa armigera.

Can mechanism help explain insect host choice

Evolutionary theory predicts that herbivorous insects should lay eggs on plants in a way that reflects the suitability of each plant species for larval development. Empirical studies, however, often fail to find any relationship between an adult insect’s choice of host–plant and offspring fitness, and in such cases, it is generally assumed that other ‘missing’ factors (e.g. predation, host–plant abundance, learning and adult feeding sites) must be contributing to overall host suitability. Here, I consider an alternative theory – that a fitness cost inherent in the olfactory mechanism could constrain the evolution of insect host selection. I begin by reviewing current knowledge of odour processing in the insect antennal lobe with the aid of a simple schematic: the aim being to explain the workings of this mechanism to scientists who do not have prior knowledge in this field. I then use the schematic to explore how an insect’s perception of host and non‐host odours is governed by a set of processing rules, or algorithm. Under the assumptions of this mechanistic view, the perception of every plant odour is interrelated, and seemingly bad host choices can still arise as part of an overall adaptive behavioural strategy. I discuss how an understanding of mechanism can improve the interpretation of theoretical and empirical studies in insect behaviour and evolution.

Discrepancy Between Antennal and Behavioral Responses for Enantiomers of α-Pinene: Electrophysiology and Behavior of Helicoverpa armigera (Lepidoptera)

The ability of adult cotton bollworm, Helicoverpa armigera (Hübner), to distinguish and respond to enantiomers of α-pinene was investigated with electrophysiological and behavioral methods. Electroantennogram recordings using mixtures of the enantiomers at saturating dose levels, and single unit electrophysiology, indicated that the two forms were detected by the same receptor neurons. The relative size of the electroantennogram response was higher for the (−) compared to the (+) form, indicating greater affinity for the (−) form at the level of the dendrites. Behavioral assays investigated the ability of moths to discriminate between, and respond to the (+) and (−) forms of α-pinene. Moths with no odor conditioning showed an innate preference for (+)-α-pinene. This preference displayed by naïve moths was not significantly different from the preferences of moths conditioned on (+)-α-pinene. However, we found a significant difference in preference between moths conditioned on the (−) enantiomer compared to naïve moths and moths conditioned on (+)-α-pinene, showing that learning plays an important role in the behavioral response. Moths are less able to distinguish between enantiomers of α-pinene than different odors (e.g., phenylacetaldehyde versus (−)-α-pinene) in learning experiments. The relevance of receptor discrimination of enantiomers and learning ability of the moths in host plant choice is discussed.

No evidence for change in oviposition behaviour of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) after widespread adoption of transgenic insecticidal cotton

Cotton growing landscapes in Australia have been dominated by dual-toxin transgenic Bt varieties since 2004. The cotton crop has thus effectively become a sink for the main target pest, Helicoverpa armigera. Theory predicts that there should be strong selection on female moths to avoid laying on such plants. We assessed oviposition, collected from two cotton-growing regions, by female moths when given a choice of tobacco, cotton and cabbage. Earlier work in the 1980s and 1990s on populations from the same geographic locations indicated these hosts were on average ranked as high, mid and low preference plants, respectively, and that host rankings had a heritable component. In the present study, we found no change in the relative ranking of hosts by females, with most eggs being laid on tobacco, then cotton and least on cabbage. As in earlier work, some females laid most eggs on cotton and aspects of oviposition behaviour had a heritable component. Certainly, cotton is not avoided as a host, and the implications of these finding for managing resistance to Bt cotton are discussed.

Host location behaviour in the desert caterpillar, Heliothis punctifera

The host location behaviour of foraging caterpillars has received little attention, despite the wealth of theoretical and empirical studies that have been directed at this behavioural trait in adult Lepidoptera. Here, we study caterpillars of the moth Heliothis punctifera Walker (Lepidoptera: Noctuidae), which inhabits the arid inland desert areas of Australia. Caterpillars of this species consume many flowerheads before completing development and can be observed moving across the sand in search of new hosts. Consequently, if host location behaviour favours attraction to certain plant species, it might be expected to influence the distribution and abundance of caterpillars in the field. We present field data showing that H. punctifera caterpillars are unevenly distributed throughout mixed patches of two of its host species, with a higher abundance on Senecio gregorii F. Muell., the annual yellow top, compared to Myriocephalus stuartii (F. Muell. & Sond.) Benth., the poached egg daisy (both Asteraceae). Using laboratory studies, we test whether this distribution may, in part, be due to host location behaviour of caterpillars. Our results show that caterpillars exhibit a preference for locating S. gregorii in their pre‐ and post‐contact foraging behaviour. In addition, our results provide evidence that feeding history plays a role in host location behaviour in this insect. We propose that key features of the desert environment and the ecology of H. punctifera would favour adaptations to host location behaviour by immatures.

Do Fruit Ripening Volatiles Enable Resource Specialism in Polyphagous Fruit Flies

Frugivorous tephritid fruit flies have lineages with high levels of host generalism. These insects use olfaction to locate fruits, but how they are able to recognize the odors of so many different host species is poorly understood. We used a series of behavioral experiments to investigate the role of fruit ripening volatiles as host cues in the Queensland fruit fly, Bactrocera tryoni (Froggatt), a polyphagous pest in Australia. Odors of mature guava (Psidium guajava) attracted female and male flies more strongly than three other ripening stages and guava pulp. We analyzed volatiles from guava odor and selected eleven compounds, all of which elicited an electrophysiological response in the antenna of female flies. Three of these, ethyl acetate, ethyl butyrate, and ethyl propionate, were released at the highest rates from the most attractive ripening stage. In behavioral trials, these three esters were not attractive individually, whereas a combination was necessary and sufficient in attracting female flies. The three-component blend was as attractive as the entire 11-component blend, which without these key volatiles was not attractive. Moreover, injecting low ranking hosts (squash and cucumber) with the three volatiles increased attraction in ovipositing female flies. These fruit flies are classed as generalists, but like many polyphagous insects they could be regarded as resource specialists, preferring specific plant reproductive stages with predictable odor cues. Exploring olfaction from this perspective could improve our understanding of host choice in polyphagous insects, and the selection of volatiles to be used as attractants in insect pest management.

Two Gut-Associated Yeasts in a Tephritid Fruit Fly have Contrasting Effects on Adult Attraction and Larval Survival

Yeast-insect interactions have been well characterized in drosophilid flies, but not in tephritid fruit flies, which include many highly polyphagous pest species that attack ripening fruits. Using the Queensland fruit fly (Bactrocera tryoni) as our model tephritid species, we identified yeast species present in the gut of wild-collected larvae and found two genera, Hanseniaspora and Pichia, were the dominant isolates. In behavioural trials using adult female B. tryoni, a fruit-agar substrate inoculated with Pichia kluyveri resulted in odour emissions that increased the attraction of flies, whereas inoculation with Hanseniaspora uvarum, produced odours that strongly deterred flies, and both yeasts led to decreased oviposition. Larval development trials showed that the fruit-agar substrate inoculated with the ‘deterrent odour’ yeast species, H. uvarum, resulted in significantly faster larval development and a greater number of adult flies, compared to a substrate inoculated with the ‘attractive odour’ yeast species, P. kluyveri, and a yeast free control substrate. GC-MS analysis of volatiles emitted by H. uvarum and P. kluyveri inoculated substrates revealed significant quantitative differences in ethyl-, isoamyl-, isobutyl-, and phenethyl- acetates, which may be responsible for the yeast-specific olfactory responses of adult flies. We discuss how our seemingly counterintuitive finding that female B. tryoni flies avoid a beneficial yeast fits well with our understanding of female choice of oviposition sites, and how the contrasting behavioural effects of H. uvarum and P. kluyveri raises interesting questions regarding the role of yeast-specific volatiles as cues to insect vectors. A better understanding of yeast-tephritid interactions could assist in the future management of tephritid fruit fly pests through the formulation of new “attract and kill” lures, and the development of probiotics for mass rearing of insects in sterile insect control programs.

From laboratory to the field: consistent effects of experience on host location by the fruit fly parasitoid Diachasmimorpha kraussii (Hymenoptera: Braconidae): Experience and host lacation in D. krausii

Associative learning is well documented in Hymenopteran parasitoids, where it is thought to be an adaptive mechanism for increasing successful host location in complex environments. Based on this learning capacity, it has been suggested that providing prerelease training to parasitoids reared for inundative release may lead to a subsequent increase in their efficacy as biological control agents. Using the fruit fly parasitoid Diachasmimorpha krausii we tested this hypothesis in a series of associative learning experiments which involved the parasitoid, two host fruits (tomatoes and nectarine), and one host fly (Bactrocera tryoni). In sequential Y‐tube olfactometer studies, large field‐cage studies, and then open field studies, naïve wasps showed a consistent preference for nectarines over tomatoes. The preference for nectarines was retained, but not significantly increased, for wasps which had prior training exposure to nectarines. However, and again consistently at all three spatial scales, prior experience on tomatoes led to significantly increased attraction to this fruit by tomato‐trained wasps, including those liberated freely in the environment. These results, showing consistency of learning at multiple spatial scales, gives confidence to the many laboratory‐based learning studies which are extrapolated to the field without testing. The experiment also provides direct experimental support for the proposed practice of enhancing the quality of inundatively released parasitoids through associative learning.