Is a mango just a mango? Testing within-fruit oviposition site choice and larval performance of a highly polyphagous fruit fly

For fruit flies, fully ripe fruit is preferred for adult oviposition and is superior for offspring performance over unripe or ripening fruit. Because not all parts of a single fruit ripen simultaneously, the opportunity exists for adult fruit flies to selectively choose riper parts of a fruit for oviposition and such selection, if it occurs, could positively influence offspring performance. Such fine scale host variation is rarely considered in fruit fly ecology, however, especially for polyphagous species which are, by definition, considered to be generalist host users. Here we study the adult oviposition preference/larval performance relationship of the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), a highly polyphagous pest species, at the “within-fruit” level to see if such a host use pattern occurs. We recorded the number of oviposition attempts that female flies made into three fruit portions (top, middle and bottom), and larval behavior and development within different fruit portions for ripening (color change) and fully-ripe mango, Mangifera indica L. (Anacardiaceae). Results indicate that female B. dorsalis do not oviposit uniformly across a mango fruit, but lay most often in the top (i.e., stalk end) of fruit and least in the bottom portion, regardless of ripening stage. There was no evidence of larval feeding site preference or performance (development time, pupal weight, percent pupation) being influenced by fruit portion, within or across the fruit ripening stages. There was, however, a very significant effect on adult emergence rate from pupae, with adult emergence rate from pupae from the bottom of ripening mango being approximately only 50% of the adult emergence rate from the top of ripening fruit, or from both the top and bottom of fully-ripe fruit. Differences in mechanical (firmness) and chemical (total soluble solids, titratable acidity, total non-structural carbohydrates) traits between different fruit portions were correlated with adult fruit utilisation. Our results support a positive adult preference/offspring performance relationship at within-fruit level for B. dorsalis. The fine level of host discrimination exhibited by B. dorsalis is at odds with the general perception that, as a polyphagous herbivore, the fly should show very little discrimination in its host use behavior.

How host plant variability influences the advantages to learning : a theoretical model for oviposition behaviour in Lepidoptera

Learning can allow individuals to increase their fitness in particular environments. The advantage to learning depends on the predictability of the environment and the extent to which animals can adjust their behaviour. Earlier general models have investigated when environmental predictability might favour the evolution of learning in foraging animals. Here, we construct a theoretical model that predicts the advantages to learning using a specific biological example: oviposition in the Lepidoptera. Our model includes environmental and behavioural complexities relevant to host selection in these insects and tests whether the predictions of the general models still hold. Our results demonstrate how the advantage of learning is maximised when within-generation variability is minimised (the local environment consists mainly of a single host plant species) and between-generation variability is maximised (different host plant species are the most common in different generations). We discuss how our results: (a) can be applied to recent empirical work in different lepidopteran species and (b) predict an important role of learning in lepidopteran agricultural pests.

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.

The functional significance of fruit exocarp on host selection and oviposition by Queensland fruit fly, Bactrocera tryoni (Froggatt) (Tephritidae: Diptera)

Queensland fruit fly is Australia's most serious insect pest of horticulture. The fly lays its eggs into fruit, where they hatch into maggots which destroy the fruit. Understanding egg laying behaviour, known as oviposition, is a critical but under-researched aspect of fruit fly biology. This thesis focused on three aspects of oviposition: the role of fruit peel as a physical barrier to oviposition; the quality of fruit for maggot development; and the structure and wear of the egg laying organ – the ovipositor. Results showed that flies selected fruit based on their suitability for offspring survival, not because of the softness or hardness of fruit peel. Previously reported use of holes or wounds in fruit peel by ovipositing females was determined to be a mechanism which saved the female time, not a mechanism to reduce ovipositor wear. The results offer insights into the evolution of host use by fruit flies and their sustainable management.

Influence of host plant structure and microclimate on the abundance and behaviour of Tephritid fly

Microclimate and host plant architecture significantly influence the abundance and behavior of insects. However, most research in this field has focused at the invertebrate assemblage level, with few studies at the single-species level. Using wild Solanum mauritianum plants, we evaluated the influence of plant structure (number of leaves and branches and height of plant) and microclimate (temperature, relative humidity, and light intensity) on the abundance and behavior of a single insect species, the monophagous tephritid fly Bactrocera cacuminata (Hering). Abundance and oviposition behavior were signficantly influenced by the host structure (density of foliage) and associated microclimate. Resting behavior of both sexes was influenced positively by foliage density, while temperature positively influenced the numbers of resting females. The number of ovipositing females was positively influenced by temperature and negatively by relative humidity. Feeding behavior was rare on the host plant, as was mating. The relatively low explanatory power of the measured variables suggests that, in addition to host plant architecture and associated microclimate, other cues (e.g., olfactory or visual) could affect visitation and use of the larval host plant by adult fruit flies. For 12 plants observed at dusk (the time of fly mating), mating pairs were observed on only one tree. Principal component analyses of the plant and microclimate factors associated with these plants revealed that the plant on which mating was observed had specific characteristics (intermediate light intensity, greater height, and greater quantity of fruit) that may have influenced its selection as a mating site.

Bactrocera dorsalis Preference for and performance on two mango varieties at three stages of ripeness

Most tropical fruit flies only lay into mature fruit, but a small number can also oviposit into unripe fruit. Little is known about the link between adult oviposition preference and offspring performance in such situations. In this study we examine the influence of different ripening stages of two mango Mangifera indica L. (Anacardiaceae) varieties on the preference and performance of the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), a fly known to be able to develop in unripe fruit. Work was carried out as a series of laboratory-based choice and no-choice oviposition experiments and larval growth trials. In oviposition choice trials, female B. dorsalis demonstrated a preference for ripe fruit of mango variety Namdorkmai over variety Oakrong, but generally the dependent variable most influencing oviposition results was fruit ripening stage. Ripe and fully-ripe mangoes were most preferred for oviposition by B. dorsalis. In contrast, unripe mango was infrequently used by ovipositing females, particularly in choice trials. Consistent with the results of oviposition preference, ripe and fully-ripe mangoes were also best for offspring survival, with a higher percentage of larval survival to pupation and shorter development times in comparison to unripe mango. Changes in Total Soluble Solids, TSS, and skin toughness correlate with changing host use across the ripening stages. Regardless of the mango variety or ripeness stage, B. dorsalis had difficulty penetrating the pericarp of our experimental fruit. Larval survival was also often poor. We discuss the possibility that there may be differences in the ability of laboratory and wild flies to penetrate fruit for oviposition, or that in the field flies more regularly utilize natural fruit wounds as oviposition sites.

Direct and indirect effects of egg parasitism by Neopolyscystus Girault sp. (Hymenoptera: Pteromalidae) on Paropsis atomaria Olivier (Coleoptera: Chrysomelidae)

Abstract Neopolycystus sp. is the only primary egg parasitoid associated with the pest beetle Paropsis atomaria in subtropical eucalypt plantations, but its impact on its host populations is unknown. The simplified ecosystem represented by the plantation habitat, lack of interspecific competition for host and parasitoid, and the multivoltinism of the host population makes this an ideal system for quantifying the direct and indirect effects of egg parasitism, and hence, effects on host population dynamics. Within-, between- and overall-egg-batch parasitism rates were determined at three field sites over two field seasons, and up to seven host generations. The effect of exposure time (egg batch age), host density proximity to native forest and water sources on egg parasitism rates was also tested. Neopolycystus sp. exerts a significant influence on P. atomaria populations in Eucalyptus cloeziana. plantations in south-eastern Queensland, causing the direct (13%) and indirect (15%) mortality of almost one-third of all eggs in the field. Across seasons and generations, 45% of egg batches were parasitised, with a within-batch parasitism rate of around 30%. Between-batch parasitism increased up to 5–6 days after oviposition in the field, although within-batch parasitism rates generally did not. However, there were few apparent patterns to egg parasitism, with rates often varying significantly between sites and seasons.

Preference among four Bactrocera species (Diptera: Tephritidae) by Diachasmimorpha kraussii (Fullaway) (Hymenoptera: Braconidae)

Diachasmimorpha kraussii is an endoparasitoid of larval dacine fruit flies. To date the only host preference study done on D. kraussii has used fruit flies from outside its native range (Australia, Papua New Guinea, Solomon Islands). In contrast, this paper investigates host preference for four fly species (Bactrocera cacuminata, B. cucumis, B. jarvisi and B. tryoni) which occur sympatrically with the wasp in the Australian component of the native range. Diachasmimorpha kraussii oviposition preference, host suitability (parasitism rate, number of progeny, sex ratio), and offspring performance measures (body length, hind tibial length, developmental time) were investigated with respect to the four fly species in the laboratory in both no-choice and choice situations. The parasitoid accepted all four fruit fly species for oviposition in both no-choice and choice tests; however, adult wasps only emerged from B. jarvisi and B. tryoni. Through dissection, it was demonstrated that parasitoid eggs were encapsulated in both B. cacuminata and B. cucumis. Between the two suitable hosts, measurements of oviposition preference, host suitability and offspring performance measurements either did not vary significantly, or varied in an inconsistent manner. Based on our results, and a related study by other authors, we conclude that D. krausii, at the point of oviposition, cannot discriminate between physiologically suitable and unsuitable hosts.

Ecology and behavior of first instar larval Lepidoptera

Neonate Lepidoptera are confronted with the daunting task of establishing themselves on a food plant. The factors relevant to this process need to be considered at spatial and temporal scales relevant to the larva and not the investigator. Neonates have to cope with an array of plant surface characters as well as internal characters once the integument is ruptured. These characters, as well as microclimatic conditions, vary within and between plant modules and interact with larval feeding requirements, strongly affecting movement behavior, which may be extensive even for such small organisms. In addition to these factors, there is an array of predators, pathogens, and parasitoids with which first instars must contend. Not surprisingly, mortality in neonates is high but can vary widely. Experimental and manipulative studies, as well as detailed observations of the animal, are vital if the subtle interaction of factors responsible for this high and variable mortality are to be understood. These studies are essential for an understanding of theories linking female oviposition behavior with larval survival, plant defense theory, and population dynamics, as well as modern crop resistance breeding programs.

Transcriptome Profiling of Sexual Maturation and Mating in the Mediterranean Fruit Fly, Ceratitis capitata

Sexual maturation and mating in insects are generally accompanied by major physiological and behavioural changes. Many of these changes are related to the need to locate a mate and subsequently, in the case of females, to switch from mate searching to oviposition behaviour. The prodigious reproductive capacity of the Mediterranean fruit fly, Ceratitis capitata, is one of the factors that has led to its success as an invasive pest species. To identify the molecular changes related to maturation and mating status in male and female medfly, a microarray-based gene expression approach was used to compare the head transcriptomes of sexually immature, mature virgin, and mated individuals. Attention was focused on the changes in abundance of transcripts related to reproduction, behaviour, sensory perception of chemical stimulus, and immune system processes. Broad transcriptional changes were recorded during female maturation, while post-mating transcriptional changes in females were, by contrast, modest. In male medfly, transcriptional changes were consistent both during maturation and as a consequence of mating. Of particular note was the lack of the mating-induced immune responses that have been recorded for Drosophila melanogaster, that may be due to the different reproductive strategies of these species. This study, in addition to increasing our understanding of the molecular machinery behind maturation and mating in the medfly, has identified important gene targets that might be useful in the future management of this pest.

Host location by the fruit fly parasitoid Diachasmimorpha krausii : role of fruit fly species, life stage and host plant

1 Diachasmimorpha krausii is a braconid parasitoid of larval tephritid fruit flies, which feed cryptically within host fruit. At the ovipositor probing stage, the wasp cannot discriminate between hosts that are physiologically suitable or unsuitable for offspring development and must use other cues to locate suitable hosts. 2 To identify the cues used by the parasitoid to find suitable hosts, we offered, to free flying wasps, different combinations of three fruit fly species (Bactrocera tryoni, Bactrocera cacuminata, Bactrocera cucumis), different life stages of those flies (adults and larvae) and different host plants (Solanum lycopersicon, Solanum mauritianum, Cucurbita pepo). In the laboratory, the wasp will readily oviposit into larvae of all three flies but successfully develops only in B. tryoni. Bactrocera tryoni commonly infests S. lycopersicon (tomato), rarely S. mauritianum (wild tobacco) but never C. pepo (zucchini). The latter two plant species are common hosts for B. cacuminata and B. cucumis, respectively. 3 The parasitoid showed little or no response to uninfested plants of any of the test species. The presence of adult B. tryoni, however, increased parasitoid residency time on uninfested tomato. 4 When the three fruit types were all infested with larvae, parasitoid response was strongest to tomato, regardless of whether the larvae were physiologically suitable or unsuitable for offspring development. By contrast, zucchini was rarely visited by the wasp, even when infested with B. tryoni larvae. 5 Wild tobacco was infrequently visited when infested with B. cacuminata larvae but was more frequently visited, with greater parasitoid residency time and probing, when adult flies (either B. cacuminata or B. tryoni) were also present. 6 We conclude that herbivore-induced, nonspecific host fruit wound volatiles were the major cue used by foraging D. krausii. Although positive orientation to infested host plants is well known from previous studies on opiine braconids, the failure of the wasp to orientate to some plants even when infested with physiologically suitable larvae, and the secondary role played by adult fruit flies in wasp host searching, are newly-identified mechanisms that may aid parasitoid host location in environments where both physiologically suitable and unsuitable hosts occur.

Five commercial citrus rate poorly as hosts of the polyphagous fruit flyBactrocera tryoni(Froggatt) (Diptera: Tephritidae) in laboratory studies

Queensland fruit fly, Bactrocera tryoni (Froggatt), is a polyphagous pest, and many citrus types are included among its hosts. While quantification of citrus host use by B. tryoni is lacking, citrus is generally considered a ‘low pressure’ crop. This paper investigates B. tryoni female oviposition preference and offspring performance in five citrus types; Murcott mandarin (Citrus reticulata), Navel orange and Valencia orange (Citrus sinensis), Eureka lemon (Citrus limon) and yellow grapefruit (Citrus paradisi). Oviposition preference was investigated in laboratory-based choice and no-choice experiments, while immature survival and offspring performance were investigated by infesting fruits in the laboratory and evaluating pupal recovery, pupal emergence and F1 fecundity. Fruit size, Brix level and peel toughness were also measured for correlation with host use. Bactrocera tryoni demonstrated an oviposition preference hierarchy among the citrus fruits tested; Murcott and grapefruit were most preferred for oviposition and lemon the least, while preference for Navel and Valencia was intermediate. Peel toughness was negatively correlated with B. tryoni oviposition preference, while no significant correlations were detected between oviposition and Brix level or fruit size. Immature survival in the tested fruit was very low. Murcott was the best host (21% pupal recovery), while all other citrus types that showed pupal recovery of 6% or lower and no pupae were recovered from Valencia orange. In pupae recovered from Navel orange and lemon, adult eclosion was greatly reduced, while in grapefruit and lemon, no eggs were recovered from F1 adults. Based on these laboratory results, many commercial citrus varieties appear to be poor hosts for B. tryoni and may pose a low post-harvest and quarantine risk. These findings need to be confirmed in the field, as they impact on both pre-harvest and post-harvest countermeasures.

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