Learning in host selection in Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae)

The effect of experience on pre- and post-alighting host selection in adult female Helicoverpa armigera was tested in an indoor flight cage, and in a large greenhouse. The moths had experienced either tobacco or tomato plants (both are hosts of H. armigera) for 3 days, or were given no experience. Individuals were then released and their host selection assessed. All individuals caught in the greenhouse were identified and tested for post-alighting acceptance on each host. Experience significantly influenced both pre- and post-alighting host selection in ovipositing moths. This modification in behaviour is attributed to 'learning', and presents the first detailed evidence for learning in moths. Possible behavioural mechanisms involved are discussed, and a hypothesis is presented regarding learning in post-alighting host acceptance. The existence of learning in H. armigera, a highly polyphagous agricultural pest, is discussed in the light of current theories on environmental predictability and the advantages of learning. Copyright 1998 The Association for the Study of Animal Behaviour.

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. 2. The present studies show that: (1) previous experience with a flowering host species increases the probability of that species being selected for nectar foraging, and (2) previous experience of a particular flower type (food source at bottom or top of the corolla tube) increases the likelihood of the food source being found when that flower type is being searched. 3. The implications of these findings for understanding the pattern of oviposition observed in wild populations of this important pest species are discussed.

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 (Hübner), 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

Discrepancy between antennal and behavioral responses for enantiomers of a-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.

Intra-specific variation for host plant use in Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae) : implications for management

The polyphagous moth Helicoverpa armigera (Hübner) is one of the world's most important agricultural pests. A number of existing approaches and future designs for management of H. armigera rely on the assumption that moths do not exhibit either genetically and/or non-genetically based variation for host plant utilization. We review recent empirical evidence demonstrating that both these forms of variation influence host plant use in this moth. The significance of this variation in H. armigera in relation to current and future pest management strategies is examined. We provide recommendations on future research needs and directions for sustainable management of H. armigera, under a framework that includes consideration of intra-specific variation for host use relevant in this and other similar pest species.

Variability in odour reception in the peripheral sensory system of Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae)

Mixtures of single odours were used to explore the receptor response profile across individual antennae of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Seven odours were tested including floral and green-leaf volatiles: phenyl acetaldehyde, benzaldehyde, β-caryophyllene, limonene, α-pinene, 1-hexanol, 3Z-hexenyl acetate. Electroantennograms of responses to paired mixtures of odours showed that there was considerable variation in receptor tuning across the receptor field between individuals. Data from some moth antennae showed no additivity, which indicated a restricted receptor profile. Results from other moth antennae to the same odour mixtures showed a range of partial additivity. This indicated that a wider array of receptor types was present in these moths, with a greater percentage of the receptors tuned exclusively to each odour. Peripheral receptor fields show variation in the spectrum of response within a population (of moths) when exposed to high doses of plant volatiles. This may be related to recorded variation in host choice within moth populations as reported by other authors.

Increased plant volatile production affects oviposition, but not larval development, in the moth Helicoverpa armigera

It is well established that herbivorous insects respond to changes in plant odour production, but little attention has been given to whether these responses relate to direct fitness costs of plant volatile production on insect growth and survival. Here, we use transgenic Nicotiana tabacum (tobacco) plants that produce relatively large amounts of the volatile (S)-linalool to study whether the responses of egg-laying herbivorous insects to linalool production relate directly to the growth and survival of offspring. In choice tests, fewer eggs were laid on transgenic plants compared with non-transformed controls, indicating that increased linalool emissions have a deterrent effect on Helicoverpa armigera oviposition. Larval survival and larval mass after feeding on transgenic leaves, however, was comparable to non-transformed controls. (S)-linalool, whether in volatile or sequestered form, does not appear to have a direct effect on offspring fitness in this moth. We discuss how the ecology of this polyphagous moth species may necessitate a high tolerance for certain volatiles and their related non-volatile compounds, and suggest that responses by adult female H. armigera moths towards increased linalool production may be context specific and relate to other indirect effects on fitness.

No evidence for change in oviposition behaviour of Helicoverpa armigera (Hubner) (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.

Complete genome sequences of Helicoverpa armigera Single Nucleopolyhedrovirus Strains AC53 and H25EA1 from Australia

We report here the genome sequences of two alphabaculoviruses of Helicoverpa spp. from Australia: AC53, used in the biopesticides ViVUS and ViVUS Max, and H25EA1, used in in vitro production studies.

Recruitment and loss of juvenile stages of Helicoverpa spp. (Lepidoptera: Noctuidae) on contaminant plants in chickpea crops

The hypothesis that contaminant plants growing amongst chickpea serve as Helicoverpa sinks by diverting oviposition pressure away from the main crop was tested under field conditions. Gain (recruitment) and loss (presumed mortality) of juvenile stages of Helicoverpa spp. on contaminant faba bean and wheat plants growing in chickpea plots were quantified on a daily basis over a 12-d period. The possibility of posteclosion movement of larvae from the contaminants to the surrounding chickpea crop was examined. Estimated total loss of the census population varied from 80 to 84% across plots and rows. The loss of brown eggs (40–47%) contributed most to the overall loss estimate, followed by loss of white eggs (27–35%) and larvae (6–9%). The cumulative number of individuals entering the white and brown egg and larval stages over the census period ranged from 15 to 58, 10–48 and 1–6 per m row, respectively. The corresponding estimates of mean stage-specific loss, expressed as a percentage of individuals entering the stage, ranged from 52 to 57% for white eggs, 87–108% for brown eggs and 71–87% for first-instar larvae. Mean larval density on chickpea plants in close proximity to the contaminant plants did not exceed the baseline larval density on chickpea further away from the contaminants across rows and plots. The results support the hypothesis that contaminant plants in chickpea plots serve as Helicoverpa sinks by diverting egg pressure from the main crop and elevating mortality of juvenile stages. Deliberate contamination of chickpea crops with other plant species merits further investigation as a cultural pest management strategy for Helicoverpa spp.

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

The ability of adult cotton bollworm, Helicoverpa armigera (Hubner), 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 naıve 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 naıve 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.

Evaluating legume species as alternative trap crops to chickpea for management of Helicoverpa spp. (Lepidoptera: Noctuidae) in central Queensland cotton cropping systems

Mounting levels of insecticide resistance within Australian Helicoverpa spp. populations have resulted in the adoption of non-chemical IPM control practices such as trap cropping with chickpea, Cicer arietinum (L.). However, a new leaf blight disease affecting chickpea in Australia has the potential to limit its use as a trap crop. Therefore this paper evaluates the potential of a variety of winter-active legume crops for use as an alternative spring trap crop to chickpea as part of an effort to improve the area-wide management strategy for Helicoverpa spp. in central Queensland’s cotton production region. The densities of Helicoverpa eggs and larvae were compared over three seasons on replicated plantings of chickpea, Cicer arietinum (L.), field pea Pisum sativum (L), vetch, Vicia sativa (L.) and faba bean, Vicia faba (L.). Of these treatments, field pea was found to harbour the highest densities of eggs. A partial life table study of the fate of eggs oviposited on field pea and chickpea suggested that large proportions of the eggs laid on field pea suffered mortality due to dislodgment from the plants after oviposition. Plantings of field pea as a replacement trap crop for chickpea under commercial conditions confirmed the high level of attractiveness of this crop to ovipositing moths. The use of field pea as a trap crop as part of an areawide management programme for Helicoverpa spp. is discussed.

Impact of mirid (Creontiades spp.) (Hemiptera: Miridae) pest management on Helicoverpa spp. (Lepidoptera: Noctuidae) outbreaks: The case for conserving natural enemies

Creontiades spp. (Hemiptera: Miridae) are sucking pests that attack buds, flowers and young pods in mungbeans, Vigna radiata (L.), causing these structures subsequently to abort. If left uncontrolled, mirids can cause 25-50% yield loss. Traditional industry practice has involved prophylactic applications of dimethoate to control mirids at budding and again a week later. The present trial was initiated to highlight the dangers of such a practice, in particular the risk of a subsequent Helicoverpa spp. lepidopteran pest outbreak. A single application of dimethoate halved the population of important natural enemies of Helicoverpa spp., and caused an above-threshold outbreak of Helicoverpa spp. within 11 days. This shows that even a moderate (e.g. 50%) reduction in natural enemies may be sufficient to increase Helicoverpa spp. populations in mungbeans. As a result, prophylactic sprays should not be used for the control of mirids in mungbeans, and dimethoate should be applied only when mirids are above the economic threshold. Indoxacarb was also tested to establish its effect on Helicoverpa spp., mirids and natural enemies. Indoxacarb showed potential for Helicoverpa spp. control and suppression of mirids and had little impact on natural enemies.

Helicoverpa armigera (Hubner): can wheat stubble protect cotton plants against attack?

When investigating strategies for Helicoverpa armigera (Hubner) control, it is important to understand oviposition behaviour. Cotton (Gossypium hirsutum) was sown into standing wheat (Triticum astivum L.) stubble in a closed arena to investigate the effect of stubble on H. armigera moth behaviour and oviposition. Infrared cameras were used to track moths and determine whether stubble acted as a physical barrier or provided camouflage to cotton plants, thereby reducing oviposition. Searching activity was observed to peak shortly before dawn (03:00 and 04:00 h) and remained high until just after dawn (4 h window). Moths spent more time resting on cotton plants than spiralling above them, and the least time flying across the arena. While female moths spent more time searching for cotton plants growing in wheat stubble, the difference in oviposition was not significant. As similar numbers of eggs were laid on cotton plants with stubble (3.5/plant SE +/- 0.87) and without stubble (2.5/plant SE +/- 0.91), wheat stubble does not appear to provide camouflage to cotton plants. There was no significant difference in the location of eggs deposited on cotton plants with and without stubble, although more eggs were laid on the tops of cotton leaves in wheat stubble. As the spatial and temporal distribution of eggs laid on the cotton plant is a crucial component of population stability, eggs laid on the upper side of leaves on cotton plants may be more prone to fatalities caused by environmental factors such as wind and rain. Therefore, although stubble did not influence the number of eggs laid, it did affect their distribution on the plant, which may result in increased mortality of eggs on cotton plants sown into standing wheat stubble.

Variability in odour reception in the peripheral sensory system of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Mixtures of single odours were used to explore the receptor response profile across individual antennae of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Seven odours were tested including floral and green-leaf volatiles: phenyl acetaldehyde, benzaldehyde, b-caryophyllene, limonene, a-pinene, 1-hexanol, 3Z-hexenyl acetate. Electroantennograms of responses to paired mixtures of odours showed that there was considerable variation in receptor tuning across the receptor field between individuals. Data from some moth antennae showed no additivity, which indicated a restricted receptor profile. Results from other moth antennae to the same odour mixtures showed a range of partial additivity. This indicated that a wider array of receptor types was present in these moths, with a greater percentage of the receptors tuned exclusively to each odour. Peripheral receptor fields show variation in the spectrum of response within a population (of moths) when exposed to high doses of plant volatiles. This may be related to recorded variation in host choice within moth populations as reported by other authors.