Polyphagy and primary host plants: oviposition preference versus larval performance in the lepidopteran pest Helicoverpa armigera

Oviposition preference and several measures of offspring performance of Helicoverpa armigera (Hübner) were investigated on a subset of its host plants that were selected for their reputed importance in the field in Australia. They included cotton, pigeon pea, sweet corn, mungbean, bean and common sowthistle. Plants were at their flowering stage when presented to gravid female moths. Flowering pigeon pea evoked far more oviposition than did the other plant species and was the most preferred plant for neonate larval feeding. It also supported development of the most robust larvae and pupae, and these produced the most fecund moths. Common sowthistle and cotton were equally suitable to pigeon pea for larval development, but these two species received far fewer H. armigera eggs than did pigeon pea. Mungbean also received relatively few eggs, but it did support intermediate measures of larval growth and survival. Fewest eggs were laid on bean and it was also the least beneficial in terms of larval growth. Among the host plant species tested, only flowering pigeon pea supported a good relationship between oviposition preference of H. armigera and its subsequent offspring performance. Australian H. armigera moths are thus consistent with Indian H. armigera moths in their ovipositional behaviour and larval performance relative to pigeon pea. The results suggest that the host recognition and acceptance behaviour of this species is fixed across its geographical distribution and they support the theory that pigeon pea might be one of the primary host plants of this insect. These insights, together with published results on the sensory responses of the females to volatiles derived from the different host plant species tested here, help to explain why some plant species are primary targets for the ovipositing moths whereas others are only secondary targets of this polyphagous pest, which has a notoriously broad host range. Handling Editor: Joseph Dickens     

Trade-offs of host use between generalist and specialist <Emphasis Type="Italic">Helicoverpa</Emphasis> sibling species: adult oviposition and larval performance

Much attention has been paid to the question of the relative importance of female behaviour versus larval feeding capacities in determining the host range of herbivorous insects. Host-use trade-offs displayed by generalist and specialist sister species of the genus Helicoverpa were evaluated to examine the relationship between maternal choice and offspring performance. The prediction of optimal oviposition theory, that females will choose to lay eggs on plants on which their offspring perform best as larvae, was tested by measuring oviposition preference and larval performance of Helicoverpa armigera and H. assulta on tobacco, sunflower, and hot pepper. These two measures were more highly correlated in the specialist H. assulta. Both species exhibited the same oviposition preference ranking: tobacco > sunflower > hot pepper. H. armigera larvae preferred sunflower, followed by tobacco and hot pepper; while H. assulta larvae preferred tobacco to sunflower and hot pepper, consistent with their mothers’ oviposition preference. Duration of the total period from egg to adult emergence for each species was significantly shorter on the host plant preferred by the larvae. H. assulta had shorter larval duration and higher relative growth rate than H. armigera on tobacco and hot pepper, and vice versa for sunflower, indicating species differences in host utilization. Thus, while only the specialist H. assulta displayed the predicted optimal oviposition pattern, females of both species show the least preference for the plant on which their offspring perform worst. Selection for optimal oviposition may be stronger on the specialist, which has fewer choices and lower lifetime fecundity than the generalist.     

Is the common sowthistle (Sonchus oleraceus) a primary host plant of the cotton bollworm,Helicoverpa armigera (Lep., Noctuidae)? Oviposition and larval performance

Helicoverpa armigera (Hübner) is a polyphagous pest that has a relatively strong affinity in the field for the European weed Sonchus oleraceus L. in parts of Australia. The oviposition preference of H. armigera was examined in relation to sowthistle and some crop hosts on which it is a pest. In a group test with simultaneous exposure of moths to common sowthistle, maize, sorghum and two cotton cultivars, H. armigera females consistently showed strongest affinities for common sowthistle, irrespective of moth age or the original host of the test insects in the field. Females ( n  = 20) exposed individually to a choice between common sothistle and cotton, varied substantially in preference. Among the females tested, 67% showed a stronger affinity for common sowthistle, about 5% preferred cotton and 28% did not discriminate. Common sowthistle was also the most preferred by newly hatched larvae among the five host plant types presented in a multiple choice test. Larvae fed on common sowthistle flowers had a higher survival rate and body weight than those fed on cotton flowers. These results and previous field observations suggest that S. oleraceus may be a primary host plant (or one of the primary host species) to which H. armigera became adapted at the time of speciation.     

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.     

HERITABILITY OF OVIPOSITION PREFERENCE AND ITS RELATIONSHIP TO OFFSPRING PERFORMANCE WITHIN A SINGLE INSECT POPULATION

Within a population of the butterfly Euphydryas editha that oviposits predominantly on two host species, heritable variation in postalighting oviposition preference was found. In a separate experiment, oviposition preference of adult females was found to be correlated with offspring performance (growth). There was a significant tendency for offspring to perform better on the host species that their female parent preferred. Analysis of the data showed that no single factor, neither maternal preference nor the host species on which the offspring were raised, accounted for any significant variation in larval performance. However, the effect of the interaction between host species and maternal preference on offspring performance was highly significant. These findings imply specialization in both oviposition preference and offspring performance by individuals within a single population. With present evidence, this preference-performance correlation is likely to be genetic. However, as in previous studies, other interpretations cannot be excluded.     

Effect of host plant on parasitism ofHelicoverpa armigera (Lep.: Noctuidae) byMicroplitis demolitor (Hym.: Braconidae)

Microplitis demolitor Wilkinson is an important larval parasitoid ofHelicoverpa armigera (Hübner) andH. punctigera (Wallengren) in Australia. The effect of host plant on parasitism of second instarH. armigera byM. demolitor was investigated in a glasshouse experiment. Parasitism was low (0%) on chickpea. Moderate to high levels of parasitism (22.4% to 75.4%) were recorded on sorghum, sunflower, maize, cotton and soybean. The results suggest that releases of larval parasitoids into chickpea are unlikely to enhance parasitismlevels during the first spring generation ofHelicoverpa spp.     

Oviposition preference and larval performance of North American monarch butterflies on four Asclepias species

Monarch butterflies, Danaus plexippus L. (Lepidoptera: Nymphalidae), occur world‐wide and are specialist herbivores of plants in the milkweed family (Asclepiadaceae). In North America, two monarch populations breed east and west of the continental divide in areas populated by different host plant species. To examine the population variation in monarch responses to different Asclepias species, we measured oviposition preference and larval performance among captive progeny reared from adult butterflies collected in eastern and western North America. Host plant use was evaluated using two milkweed species widely distributed in eastern North America (A. incarnata and A. syriaca), and two species common to western North America (A. fascicularis and A. speciosa). We predicted that exposure to different host plant species in their respective breeding ranges could select for divergent host use traits, so that monarchs should preferentially lay more eggs on, and larvae should perform better on, milkweed species common to their native habitats. Results showed that across all adult female butterflies, oviposition preferences were highest for A. incarnata and lowest for A. fascicularis, but mean preferences did not differ significantly between eastern and western monarch populations. Larvae from both populations experienced the highest survival and growth rates on A. incarnata and A. fascicularis, and we again found no significant interactions between monarch source population and milkweed species. Moreover, the average rank order of larval performance did not correspond directly to mean female oviposition preferences, suggesting that additional factors beyond larval performance influence monarch oviposition behavior. Finally, significant family level variation was observed for both preference and performance responses within populations, suggesting an underlying genetic variation or maternal effects governing these traits.     

Field performance and seasonal changes in the efficacy against Helicoverpa armigera (Hübner) of transgenic cotton expressing the insecticidal protein vip3A

1 Three years of field experiments in Eastern Australia were carried out on transgenic cotton (Gossypium hirsutum L.) event Cot102 expressing the insecticidal protein gene vip3A from Bacillus thuringiensis to evaluate performance against Helicoverpa armigera Hübner. Efficacy, defined as the capacity of plant tissues to induce larval mortality, was determined with a well‐validated leaf bioassay fortnightly through the growth cycle of the cotton in each season. 2 Cot102 plants proved highly efficacious against H. armigera, particularly early in the season, although their efficacy declined as the season progressed, in a manner similar to, but not as dramatic as, that observed with commercial Cry1Ac expressing cotton (Bollgard or Ingard cotton). 3 Field surveys indicated that very few larvae survived beyond first instar on intact growing plants. 4 In one season efficacy declined for a period of approximately 20 days after a cool wet period, suggesting that this may have had a detrimental effect on the expression or efficacy of the gene, but this will need to be verified in further replicated trials. 5 Quantitative enzyme‐linked immunosorbent assays indicated that there was no dramatic reduction in production of the vip3A protein during growth and maturation of the crop, suggesting that other host plant factors were affecting the efficacy of the insecticidal protein in the insect gut. 6 These data indicate that Cot102 cotton would provide a useful alternative to Bollgard cotton but, given the similar lytic mode of action of vip3A proteins in the insect midgut, there may be similar inherent vulnerabilities to resistance evolution for these proteins if used alone. Pyramiding of the vip3A trait with a second insecticidal gene would appear to be a high priority for achieving sustainable deployment against H. armigera or similar susceptible species.     

Butterfly oviposition preference is not related to larval performance on a polyploid herb

The preference–performance hypothesis predicts that female insects maximize their fitness by utilizing host plants which are associated with high larval performance. Still, studies with several insect species have failed to find a positive correlation between oviposition preference and larval performance. In the present study, we experimentally investigated the relationship between oviposition preferences and larval performance in the butterfly Anthocharis cardamines. Preferences were assessed using both cage experiments and field data on the proportion of host plant individuals utilized in natural populations. Larval performance was experimentally investigated using larvae descending from 419 oviposition events by 21 females on plants from 51 populations of two ploidy types of the perennial herb Cardamine pratensis. Neither ploidy type nor population identity influenced egg survival or larval development, but increased plant inflorescence size resulted in a larger final larval size. There was no correlation between female oviposition preference and egg survival or larval development under controlled conditions. Moreover, variation in larval performance among populations under controlled conditions was not correlated with the proportion of host plants utilized in the field. Lastly, first instar larvae added to plants rejected for oviposition by butterfly females during the preference experiment performed equally well as larvae growing on plants chosen for oviposition. The lack of a correlation between larval performance and oviposition preference for A. cardamines under both experimental and natural settings suggests that female host choice does not maximize the fitness of the individual offspring.     

Oviposition and feeding avoidance in Helicoverpa armigera (Hübner) against transgenic Bt cotton

Helicoverpa armigera (Hübner), the major target pest of transgenic Bacillus thuringiensis (Bt) cotton, remains susceptible to Bt cotton in China at present. Behavioural avoidance by ovipositing females might lead to reduced exposure to Bt cotton and minimize selection for physiological resistance. We examined the behavioural responses of H. armigera to Bt and non‐Bt cottons to determine whether behavioural avoidance to Bt cotton may be present. In oviposition choice tests, the number of eggs on non‐Bt cotton plants was significantly higher than on Bt cotton plants. Similarly, in no‐choice tests, Bt cotton plants attracted significantly fewer eggs compared with non‐Bt cotton plants. H. armigera neonates showed higher dispersal and lower establishment on Bt cotton than on non‐Bt cotton. First instars were found to feed consistently on non‐Bt cotton leaves, creating large feeding holes, but only produced tiny feeding holes on Bt cotton leaves. The H. armigera population used in this study showed avoidance of oviposition and feeding on Bt cotton. Our results provide important insights into one possible mechanism underlying the durability of Bt cotton resistance and may be useful for improving strategies to sustain the effectiveness of Bt crops.     

Natal origin affects host preference and larval performance relationships in a tritrophic system

Many insects face the challenge to select oviposition sites in heterogeneous environments where biotic and abiotic factors can change over time. One way to deal with this complexity is to use sensory experiences made during developmental stages to locate similar habitats or hosts in which larval development can be maximized. While various studies have investigated oviposition preference and larval performance relationships in insects, they have largely overlooked that sensory experiences made during the larval stage can affect such relationships. We addressed this issue by determining the role of natal experience on oviposition preference and larval performance relationships in a tritrophic system consisting of Galerucella sagittariae, feeding on the two host plants Potentilla palustris and Lysimachia thyrsiflora, and its larval parasitoid Asecodes lucens. We firstly determined whether differences in host‐derived olfactory information could lead to divergent host selection, and secondly, whether host preference could result in higher larval performance based on the natal origin of the insects. Our results showed that the natal origin and the quality of the current host are both important aspects in oviposition preference and larval performance relationships. While we found a positive relationship between preference and performance for natal Lysimachia beetles, natal Potentilla larvae showed no such relationship and developed better on L. thyrsiflora. Additionally, the host selection by the parasitoid was mainly affected by the natal origin, while its performance was higher on Lysimachia larvae. With this study, we showed that the relationship between oviposition preference and larval performance depends on the interplay between the natal origin of the female and the quality of the current host. However, without incorporating the full tritrophic context of these interactions, their implication in insect fitness and potential adaptation cannot be fully understood.     

Biology and fertility life table of Helicoverpa armigera (Lepidoptera: Noctuidae) in different hosts

In 2013, the presence of Helicoverpa armigera (Hübner) was reported in cotton, soybean, corn and weeds in diverse regions of Brazil. We studied the biology and the fertility life table of this pest when reared on cotton (293 cv. CNPA RF), soybean (cv. Brasmax Power), corn (cv. BRS 1010), wheat (cv. BR 18) and on an artificial diet. Caterpillars were reared using the vegetative and reproductive structures of the hosts, under laboratory conditions (temperature 25 ± 1°C; relative humidity (RH) 70 ± 10%; photoperiod =14 h). The experimental design was completely randomized, with five treatments (four host plants and artificial diet) and 17 replications. Significant effects were verified for the different types of hosts tested on the growth of the insect as well as on fecundity and laying rate. The results showed that cotton and soybean had higher viability at the stages of growth, higher rate of survival of adult females in the reproductive period than the other host crops, and similar values for insects reared on an artificial diet, which reveals that cotton and soybean can be appropriate for rearing H. armigera on a natural diet. Corn and wheat showed high larval and pupal mortality and low biotic potential.     

Pupal diapause of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) mediated by larval host plants: pupal weight is important

Facultative diapause, a strategy that allows insects to initiate additional generations when conditions are favorable or to enter diapause when they are not, has a profound effect on the ecology and evolution of species. Most previous studies have concentrated on the role of photoperiod and temperature in inducing facultative diapause in insects. In contrast, here we studied pupal diapause mediated by larval host plants in the cotton bollworm Helicoverpa armigera, and confirmed that pupal weight is a critical factor. Two groups of third instar H. armigera larvae, kept at 25 °C with L:D = 8:16 and 20 °C with photoperiod of L:D = 8:16, respectively, were fed on six host plants and on artificial diet (as a control) to determine how larval host plants affect diapause incidence and related traits (such as pupal weight and developmental duration). The data showed larval host plants affected diapause incidence significantly and the effects could be masked by low temperature. Further analysis showed that pupal size, not the length of the sensitive stage, affected the decision to enter diapause. In a further experiment, third-instar to final-stage larvae deprived of artificial diet for 2 days demonstrated a direct relationship between pupal weight and diapause incidence. These results suggest that larval host plants, by affecting pupal size, may influence diapause occurrence in H. armigera. This has important adaptive significance for both over-wintering survival and the possibility for completing an additional generation.     

Butterflies and plants: preference/performance studies in relation to plant size and the use of intact plants vs. cuttings

Plants have evolved a number of defences to ameliorate herbivore attacks including chemicals induced by mechanical wounding. Such changes in plant chemical composition are potential confounding factors in experiments on plant – insect interactions, which often present cuttings of potential host plants to phytophagous insects. In particular, this could affect studies of female egg‐laying preference and larval performance, because the same plant chemicals that deter certain generalist insects can elevate attacks from more specialized insects. Furthermore, plant cuttings are by definition smaller than intact plants, and any female host size preference could thus affect experiments using plant cuttings. We first assessed female preference and larval performance of a specialist herbivore, Pieris napi (L.) (Lepidoptera: Pieridae, Pierini), confronted with either intact plants or leaf‐cuttings of four Brassicaceae host plants, Alliaria petiolata (Bieb.) Cavara & Grande, Barbarea vulgaris (L.) WT Aiton, Berteroa incana (L.) DC., and Brassica napus (L.). Egg and larval survival did not differ between intact plants and leaf‐cuttings, whereas larval growth was slightly, but significantly, faster on leaf‐cuttings. Females, however, significantly preferred to lay eggs on intact plants of all four hosts, although the preference hierarchy for the intact plants was largely mirrored by that for leaf‐cuttings. We then tested the female preference for different size‐classes of intact B. napus plants. Small individuals received more eggs than larger individuals, and follow‐up experiments showed that this difference was largely generated by a strong female preference for cotyledon leaves; there was no significant difference in female preference for large and small individuals when both carried cotyledons, and females landing on cotyledons were more likely to oviposit compared to when landing on a true leaf. Our study concludes that plant cuttings can serve as adequate proxies for live plants for preference/performance studies, but that experimentalists should be aware of the variation imposed both by plant handling and plant phenology for female oviposition preference.     

Vetiver grass (Vetiveria zizanioides (L.) Nash) as trap plant for Chilo partellus (Swinhoe) (Lepidoptera: Pyralidae) and Busseola fusca (Fuller) (Lepidoptera: Noctuidae)

The preference of lepidopterous stem borer moths to oviposit on certain wild host plants can be exploited in habitat management systems by using those hosts as trap crops. Vetiver grass (Vetiveria zizanioides (L.) Nash) was evaluated for its attractiveness and suitability to the pyralid Chilo partellus (Swinhoe) (Lepidoptera: Pyralidae) and the noctuid Busseola fusca (Fuller) (Lepidoptera: Noctuidae). Two choice tests were conducted in the laboratory and in the greenhouse to determine oviposition choice of C. partellus for maize, Vetiver and rice (Oryza sativa L.), and of B. fusca for Vetiver and maize. C. partellus larval survival was evaluated in green house studies. Results indicated that C. partellus chose Vetiver grass over maize though larval survival on Vetiver was extremely low. B. fusca did not show any host preference.     

The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis

1. A series of experiments was conducted to measure the impact of plant genotype, plant growth rate, and intraspecific competition on the oviposition preference and offspring performance of the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and Solidago gigantea (Asteraceae). Previous research has shown that both host races prefer to oviposit on their own host plant where survival is much higher than on the alternate host plant. In this study, neither host race showed any relationship between oviposition preference and offspring performance in choosing among plants of their natal host species. 2. The larval survival of both host races differed among plant genotypes when each host race oviposited on its natal host species. In one experiment, altissima host race females showed a preference among plant genotypes that was not correlated with offspring performance on those genotypes. In all other experiments, neither the altissima nor gigantea host race demonstrated a preference for specific host plant genotypes. 3. Eurosta solidaginis had a preference for ovipositing on rapidly growing ramets in all experiments, however larval survival was not correlated with ramet growth rate at the time of oviposition. 4. Eurosta solidaginis suffered high mortality from intraspecific competition in the early larval stage. There was little evidence, however, that females avoided ovipositing on ramets that had been attacked previously. This led to an aggregated distribution of eggs among ramets and strong intraspecific competition. 5. There was no interaction among plant genotype, plant growth rate, or intraspecific competition in determining oviposition preference or offspring performance.     

Bottom-up effects of Brassica napus nutrition on the oviposition preference and larval performance of Ceutorhynchus obstrictus (Coleoptera: Curculionidae)

The cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), is a serious pest of canola, Brassica napus L. and Brassica rapa L., both in Europe and North America. Nitrogen and sulfur levels can be readily manipulated by growers and could potentially be exploited to improve current pest management strategies. In an effort to better understand the relationship between host plant nutrition and C. obstrictus oviposition preference and its larval developmental biology, we exposed gravid females to host plants grown under differing regimes of nitrogen and sulfur. Results indicated that plants grown with a higher supply of nitrogen were preferred as hosts. Plants with a higher sulfur supply were also preferred but only in plants grown at lower nitrogen levels. In contrast, larval development time increased with increasing nitrogen levels although larval dry weights were unaffected. The results were inconsistent with the preference-performance hypothesis. The inconsistencies between oviposition choice and larval growth and development may be due to a conflict between maternal and larval fitness. Observed changes in larval development time may not represent a significant fitness cost for larval C. obstrictus, as no corresponding change in larval weight was observed. Possible causal mechanisms for the increase in development time include differences in oil, protein and glucosinolate contents of the seed. Fertilizer management regimes currently recommended were considered to be optimal for management of C. obstrictus as the yield benefits from higher rates of nitrogen fertilization would more than compensate for increased level of infestation.     

Oviposition dynamics and larval development of Helicoverpa armigera on a highly preferred unsuitable host plant,Solanum viarum

Oogenesis and oviposition dynamics of female moths of tomato fruitworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), were compared in a monoculture of tomato (Solanum lycopersicum L.) and in mixtures with a highly preferred but unsuitable host plant, Solanum viarum Dunal. Female H. armigera provided with S. viarum laid many more eggs than those provided with tomato, both in choice and no‐choice experiments. Gravid female moths did not display any preference for oviposition neither between young or old plants of S. viarum or tomato, nor between young and old leaves of S. viarum. Larval mortality and larval developmental period significantly increased, with subsequent reduction in pupal weight, when H. armigera larvae fed on S. viarum leaves compared to a meridic diet. Oviposition of female moths significantly increased in tomato in the presence of S. viarum volatiles. However, in screen cages with an increasing percentage of S. viarum as a trap crop, the number of eggs laid on tomato as the main crop was the same. The results of this study are discussed in light of the possibility of using S. viarum as a ‘dead‐end’ trap crop.     

Oviposition preference,larval performance and adaptation of Trichoplusia ni on cabbage and cotton

Most female herbivores ensure to lay eggs where their offspring can develop successfully. The oviposition preferences of females affect strategies in pest management. In this study, the performance of two cohorts of Trichoplusia ni larvae on cabbage and cotton (after they had been transferred from their original host plants) were investigated. The preferences of female moth ovipositing and larval feeding on these two host plants were observed. The results indicated that plants significantly affected oviposition preference of the female adults and development and survival of larvae of T. ni. All females preferred to lay eggs on cabbage than cotton regardless from which host they originated. The detrimental effects of cotton on the development and survival of T. ni larvae originated from cabbage (CaTn) increased with the increase of the larval age when they were transferred. In addition, the host plant change did not significantly affect the development and survival of larvae of T. ni originating from cotton (CoTn). Larvae of CaTn preferred cabbage plants as compared to cotton plants, whereas larvae of CoTn did not show a significant choice. Although the adult females preferred laying eggs on cabbage, they did not show preferences between cotton and cabbage in a Y‐tube olfactometer test. The hypothesis of oviposition preference and performance of larvae was supported by the results of CaTn, whereas they not supported by those from CoTn. Based on these results, the strategy to manage this serious pest was discussed.     

棉铃虫对三氟氯氰菊酯的抗性狭义遗传力及其与体重的相关性

利用数量遗传学方法和半同胞交配设计,测定了棉铃虫Helicoverpa armigera对三氟氯氰菊酯抗性和体重的狭义遗传力,并分析了棉铃虫抗药性与其体重之间的相关性。结果表明,棉铃虫对三氟氯氰菊酯的抗性狭义遗传力为0.2476±0.0248,体重遗传力为0.3613 ± 0.1299;抗性与其母体效应无关;抗性与体重之间存在显著的遗传负相关。