Oviposition,larval preference,and larval performance in two polyphagous species: does the larva know best?

It is expected that females preferentially oviposit on plant hosts that allow for optimal larval performance. However, this expectation contradicts empirical evidence where adults do not always choose the best host for their descendants. Recent evidence suggests that females’ host selection depends on the number of potential hosts. Females from oligophagous species seem to be able to choose an appropriate host in terms of larval performance, whereas in polyphagous species, adult oviposition preference is not related with larval performance. This suggests that larvae in polyphagous species could be taking a more active role in host selection than their mothers. Here, we evaluated the oviposition preference and the larval preference and performance of two polyphagous species of economic importance, Copitarsia decolora (Guenée) (Lepidoptera: Noctuidae: Cuculliinae) and Peridroma saucia (Hübner) (Lepidoptera: Noctuidae: Noctuinae), on eight species of cultivated plants. In laboratory and greenhouse choice assays, we tested adult preference for oviposition and larval preference at 1 and 24 h. Larval performance was measured in terms of survival to adulthood, length of larval period, and pupal weight. We found that both adult females and larvae actively choose their hosts and that the larval preference toward the hosts is related to the females’ preference in both herbivore species. However, the females and larvae did not preferentially select the host with the best larval performance, indicating that larval performance is not related to female or larval preference and that other selective pressures are influencing the choice of the host plant in these two species.     

Life-history strategy in an oligophagous tephritid: the tomato fruit fly, Neoceratitis cyanescens

Abstract.  1. In phytophagous insects, life-history traits mainly depend on host plant range. Substantial longevity, high fecundity and larval competition are the major traits of polyphagous Tephritidae while species with a restricted host range generally exhibit a lower longevity and fecundity as well as mechanisms to avoid larval competition. Our aim in this study was to investigate the life history of an oligophagous species, the tomato fruit fly, Neoceratitis cyanescens (Bezzi).
2. We determined life tables under laboratory conditions in order to calculate the main demographic parameters of N. cyanescens and studied the influence of larval and adult diet on life-history traits.
3. The mean longevity of N. cyanescens females was 40 days. There was a strong synchronisation of female maturity. Oviposition showed an early peak at 9–13 days after a short pre-oviposition period (6 days). The absence of proteins in the adult diet both delayed ovarian maturation and decreased female fecundity. In addition, females originating from tomato fruits produced significantly more eggs than females originating from bugweed or black nightshade, showing that even the larval host plant may strongly affect the subsequent fecundity of adult females.
4. The traits of N. cyanescens are then discussed in the light of those documented for polyphagous and monophagous tephritids. Neoceratitis cyanescens displayed attributes intermediate between those of polyphagous and monophagous tephritids. Its smaller clutch size compared with polyphagous species and its specialisation on the Solanaceae family whose fruits contain toxic compounds may help in reducing intra- and inter-specific competition, respectively.     

Feeding patterns of monophagous,oligophagous, and polyphagous insect herbivores: The effect of resource abundance and plant chemistry

Summary Leaf tissue preferences of monophagous, oligophagous, and polyphagous insect herbivores were determined using young and mature leaf tissue abundances and herbivore feeding observations. Larvae of monophagous and oligophagous herbivores preferred young leaf tissues while, overall, larvae of polyphagous species preferred mature leaves of their various host plants. Even though a species is often polyphagous over its geographical range, larvae from local populations may be very specialized in their diet. When this occurs these specialized larvae prefer the more nutritious and perhaps more toxic young leaves of some of their host plants. Resource abundance and plant chemistry are discussed as major factors influencing herbivore feeding patterns.     

棉铃虫低龄幼虫对花香挥发物的联系性学习

鳞翅目昆虫的寄主选择主要是成虫的任务,但幼虫也可以精细调节取食部位。低龄幼虫记忆一些与食物伴随的化学信息能够提高适合度。当幼虫被迫离开寄主植物后,最好是搜索与此前取食过的寄主气味相似的植物,以便节省寄主转移的生理代谢成本。棉铃虫幼虫嗜食作物花器,因此推测花香挥发物可以代表幼虫食物的典型化学信息。采用人工饲料为无条件刺激,在条件化训练开始时,使初孵幼虫取食时暴露在7种花香挥发物下,随后7 d逐日测试低龄幼虫学习表现。结果发现,在7次测试中,苯乙醛选择频次有3次显著多于对照,芳樟醇条件化组在2次测定中处理被选频次显著或极显著多于对照,苯乙醇条件化组仅1次对处理选择频次显著多于对照,其他4种挥发物无论训练时间长短均不能造成嗅觉偏好性的改变,说明棉铃虫在取食过程中是选择性采集食物关键化学信息。然而,无经历组无论训练时间如何均不对苯乙醛表现出嗅觉偏好性,证实气味偏好性的改变并非生理性成熟所致。总之,和同种的成虫以及若虫期比较活泼的其他种类相比,棉铃虫低龄幼虫嗅觉联系性学习表现较差,并且嗅觉偏好性变化与条件化训练时长没有明确关系,结合棉铃虫的生态学习性讨论了可能的原因。     

The Role of Olfactory Cues for the Search Behavior of a Specialist and Generalist Butterfly

Searching for resources is often a challenging task, especially for small organisms such as insects. Complex stimuli have to be extracted from the environment and translated into a relevant behavioral output. A first step in this process is to investigate the relative roles of the different senses during search for various resources. While the role of olfaction is well documented in nocturnal moths, the olfactory abilities of the closely related diurnal butterflies are poorly explored. Here we investigated how olfactory information is used in the search for host plants and asked if these abilities varied with levels of stimulus complexity. Thus, we tested two nymphalid butterfly species with divergent host plant range in a two-choice olfactometer testing different combinations of host and non-host plants. The experiments show both the monophagous Aglais urticae and the polyphagous Polygonia c-album could navigate towards an odor source, but this ability varied with context. While mated females exhibited a preference for their host plant, unmated females of both species did not show a preference for host plant cues. Furthermore, both species showed inabilities to make fine-tuned decisions between hosts. We conclude that olfactory cues are important for butterflies to navigate towards targets. We argue that there are limitations on how much information can be extracted from host volatiles. These results are discussed in the light of neural processing limitations and degree of host plant specialization, suggesting the necessity of other sensory modalities to sharpen the decision process and facilitate the final oviposition event.     

Host plant use in sympatric closely related flea beetles

Studies on strategies of host plant use in sympatric-related species are significant to the theory of sympatric speciation. Altica fragariae Nakane and Altica koreana Ogloblin are sympatric closely related flea beetles found in Beijing, northern China. All their recorded host plants are in the subfamily Rosoideae of the Rosaceae, so we regard them as a model system to study interactions between herbivorous insects and plant-insect co-evolution. We conducted a set of experiments on the host preference and performance of these flea beetles to study whether these closely related species have the ability to use sympatric novel host plants and whether monophagous and oligophagous flea beetles use the same strategy in host plant use. Oviposition preference experiments showed that A. koreana, a monophagous flea beetle, displayed high host fidelity. However, A. fragariae, which is oligophagous, often made "oviposition mistakes," ovipositing on nonhost plants such as Potentilla chinensis, the host plant of A. koreana, although normal host plants were preferred over novel ones. Larval performance studies suggested that A. fragariae was able to develop successfully on P. chinensis. Feeding experiences of larvae had no effect on feeding preference, oviposition preference, and fecundity of adults. However, females were impaired in their reproductive ability when fed on nonhost plants. Therefore, A. fragariae finished their development of larval stages on P. chinensis and came back to their primary host plant, Duchesnea indica, for feeding and reproduction after eclosion.     

VARIATION IN PREFERENCE AND SPECIFICITY IN MONOPHAGOUS AND OLIGOPHAGOUS SWALLOWTAIL BUTTERFLIES

Although variation in oviposition preference and specificity for host plants has been demonstrated within populations of a variety of oligophagous insect species, it is unknown whether genetic variation in host choice is lost within populations of monophagous species. Analysis of a locally monophagous butterfly species, Papilio oregonius, and a locally oligophagous species, P. zelicaon, showed significant variation in oviposition preference within populations of both species. Females of both species chose primarily their native hosts. Nonetheless, the percentages of eggs laid by individual females among the plant species and the number of plant species on which individual females laid eggs differed significantly among isofemale strains within populations. Moreover, some females within all isofemale strains of both species laid a few eggs on Foeniculum vulgare, an umbelliferous species that does not occur in the native habitats of these populations but is a host for Papilio species in other geographic areas. The results suggest that local monophagy and oligophagy in these species reflect the relative ranking among potential plant species. Both populations harbor variation in oviposition choice that could allow for host shifts if these populations invaded new habitats.     

Relationship between adult and larval host plant selection and larval performance in the generalist moth, Trichoplusia ni

Adult oviposition preferences are expected to correlate with host plant suitability for the development of their offspring. For most lepidopteran species, this is particularly important as the hatching neonate larvae of many species are relatively immobile. Thus, the site of oviposition chosen by a female adult can greatly influence the probability of survival for her offspring. In the present study, we investigated the oviposition preference of adult Trichoplusia ni moths for six plant species to determine whether they could accurately rank the suitability of the plants for larval development. We also compared oviposition preferences to neonate larval acceptance and preference to determine whether the adult host range matched that of larval diet breath. Our results indicate that in two-choice and no-choice tests adult T. ni were able to rank the plants accurately, with the exception of anise hyssop. However, when given a choice of all six plants together, they laid more eggs on a plant that was not suitable for larval survival. Larvae accepted and fed on all plants in no-choice tests, and accurately ranked them according to larval performance. We conclude that neonate larvae are better able than adults to rank plants according to larval performance, and that larval diet breadth is wider than the range of plants accepted by adults. We also provide a discussion of the reduced accuracy of adult oviposition preference with increased plant choices.     

Butterfly community structure in fragmented habitats

We analysed effects of habitat fragmentation on the diversity, abundance, and life history traits of butterflies on 33 calcareous grasslands. Diversity of butterflies was positively correlated with habitat area (as was plant diversity), but not with habitat isolation. In contrast to expectations, butterfly densities of polyphagous and oligophagous species declined with habitat area whereas densities of monophagous species increased. The z -values, i.e. the slope of species–area relationships, increased with food plant specialization, from 0.07 in polyphagous, 0.11 in oligophagous, 0.16 in strongly oligophagous to 0.22 in monophagous species, and were 0.14 in plant species. Significant z -values were not only found for total species richness, based on a sample size adjusted to fragment area ( z  = 0.12), but also for the local density of butterfly species richness, based on equal sample size across all habitat fragments ( z  = 0.06). To our knowledge, this is the first study to show differential responses of monophagous, oligophagous and polyphagous species to area with respect to species richness and population density.     

The Influence of Learning on Host Plant Preference in a Significant Phytopathogen Vector,Diaphorina citri

Although specialist herbivorous insects are guided by innate responses to host plant cues, host plant preference may be influenced by experience and is not dictated by instinct alone. The effect of learning on host plant preference was examined in the Asian citrus psyllid, Diaphorina citri; vector of the causal agent of citrus greening disease or huanglongbing. We investigated: a) whether development on specific host plant species influenced host plant preference in mature D. citri; and b) the extent of associative learning in D. citri in the form of simple and compound conditioning. Learning was measured by cue selection in a 2-choice behavioral assay and compared to naïve controls. Our results showed that learned responses in D. citri are complex and diverse. The developmental host plant species influenced adult host plant preference, with female psyllids preferring the species on which they were reared. However, such preferences were subject to change with the introduction of an alternative host plant within 24–48 hrs, indicating a large degree of experience-dependent response plasticity. Additionally, learning occurred for multiple sensory modalities where novel olfactory and visual environmental cues were associated with the host plant. However, males and females displayed differing discriminatory abilities. In compound conditioning tasks, males exhibited recognition of a compound stimulus alone while females were capable of learning the individual components. These findings suggest D. citri are dynamic animals that demonstrate host plant preference based on developmental and adult experience and can learn to recognize olfactory and visual host plant stimuli in ways that may be sex specific. These experience-based associations are likely used by adults to locate and select suitable host plants for feeding and reproduction and may suggest the need for more tailored lures and traps, which reflect region-specific cultivars or predominate Rutaceae in the area being monitored.     

Evolutionary responses by butterflies to patchy spatial distributions of resources in tropical environments

The greatest diversity of butterflies and their host plants occurs in tropical regions. Some groups of butterflies in the tropics exhibit monophagous feeding in the larval stage, exploiting only one family of plants; others are polyphagous, feeding on plants in two or more distinct families. The two major types of tropical habitats for butterflies, namely primary and secondary forests, offer very different evolutionary opportunities for the exploitation of plants as larval food. Butterflies are faced with the major logistical problem, as are many other herbivorous insects, of depositing eggs on the correct plant for successful larval feeding. This paper, using the concepts of phenotype set and spatial patchiness of resources, attemps to make some predictions as to the optimal phenotypic systems for monophagous and polyphagous feeding in tropical butterflies, as related to the spatial patchiness of larval host plants in primary and secondary forests. In addition to the secondary compound chemistry of larval host plants as playing a role in the evolution of monophagy and polyphagy, the assumption is made that the spatial patchiness of host plants within and among different families also acts as a major factor in determining optimal ranges of phenotypes for different patterns of larval feeding. Owing to the high spatial patchiness of primary forest species of canopy trees and vines, it is predicted that butterflies exploiting these will be mostly polyphagous, whereas secondary forests having stable formations of fewer plant species and larger patches of these plants, will have mostly monophagous species. Forest understories may have both monophagous and polyphagous species, depending upon the layer of forest and the general type of understory (i.e. palmaceous or dicotyledonous). Field data on some groups of butterflies from tropical America support these predictions. Polyphagous butterflies are predicted to possess a genetic system of mixed morphs with a population being polymorphic as a whole; monophagous butterflies are predicted to have individuals all more or less similar genetically, and with a high amount of genic variation within individuals. Other forms of monophagy may evolve in species that are essentially monomorphic but with various mechanisms (physiological, developmental, behavioral) of phenotypic flexibility at the individual level. Although the environment is essentially coarse-grained for larvae since most are sedentary and polymorphism is an optimal adaptive strategy, the oviposition strategy of the adult must also be considered and some situations (i.e. forest canopy) have resources (host plants) distributed in a fine-grained fashion. Other forms of limited polyphagy may result from monomorphic genetic systems in which there is considerable phenotypic flexibility.     

Ontogenetic changes in responses to settlement cues by Anemonefish

Population connectivity for most marine species is dictated by dispersal during the pelagic larval stage. Although reef fish larvae are known to display behavioral adaptations that influence settlement site selection, little is known about the development of behavioral preferences throughout the larval phase. Whether larvae are attracted to the same sensory cues throughout their larval phase, or exhibit distinct ontogenetic shifts in sensory preference is unknown. Here, we demonstrate an ontogenetic shift in olfactory cue preferences for two species of anemonefish, a process that could aid in understanding both patterns of dispersal and settlement. Aquarium-bred na?ve Amphiprion percula and A. melanopus larvae were tested for olfactory preference of relevant reef-associated chemical cues throughout the 11-day pelagic larval stage. Age posthatching had a significant effect on the preference for olfactory cues from host anemones and live corals for both species. Preferences of olfactory cues from tropical plants of A. percula, increased by approximately ninefold between hatching and settlement, with A. percula larvae showing a fivefold increase in preference for the olfactory cue produced by the grass species. Larval age had no effect on the olfactory preference for untreated seawater over the swamp-based tree Melaleuca nervosa, which was always avoided compared with blank seawater. These results indicate that reef fish larvae are capable of utilizing olfactory cues early in the larval stage and may be predisposed to disperse away from reefs, with innate olfactory preferences drawing newly hatched larvae into the pelagic environment. Toward the end of the larval phase, larvae become attracted to the olfactory cues of appropriate habitats, which may assist them in identification of and navigation toward suitable settlement sites.     

The role of female search behaviour in determining host plant range in plant feeding insects: a test of the information processing hypothesis

Recent theoretical studies have suggested that host range in herbivorous insects may be more restricted by constraints on information processing on the ovipositing females than by trade-offs in larval feeding efficiency. We have investigated if females from polyphagous species have to pay for their ability to localize and evaluate plants from different species with a lower ability to discriminate between conspecific host plants with differences in quality. Females of the monophagous butterflies Polygonia satyrus, Vanessa indica and Inachis io and the polyphagous P. c-album and Cynthia cardui (all in Lepidoptera, Nymphalidae) were given a simultaneous choice of stinging nettles (Urtica dioica) of different quality. In addition, the same choice trial was given to females from two populations of P. c-album with different degrees of specificity. As predicted from the information processing hypothesis, all specialists discriminated significantly against the bad quality nettle, whereas the generalists laid an equal amount of eggs on both types of nettle. There were no corresponding differences between specialist and generalist larvae in their ability to utilize poor quality leaves. Our study therefore suggests that female host-searching behaviour plays an important role in determining host plant range.     

Ecological and taxonomic trends in macrolepidopteran host plant selection

Patterns of host plant use by larvae of macrolepidoptera feeding on trees and shrubs in Britain and Canada are examined. The incidence of polyphagous species varies among different lepidopteran taxa. Among largely monophagous taxa host plant switching has often occurred. The greater similarity of insect faunas on closely related plants is documented using cluster analysis. The Canadian data reveal that lepidopterans feeding on conifers are less specific in their host plant choice than species feeding on angiosperms. The numerical analyses also provide evidence of greater overlap in the insect faunas of plants belonging to the same ecological association. These results are discussed with particular reference to Lepidoptera-plant coevolution.     

Food acceptance by a monophagous and an oligophagous insect in relation to seasonal changes in host plant suitability

Food acceptance by larvae of two lepidopteran species feeding on Rosaceae, viz. Yponomeuta evonymellus (monophagous) and Y. padellus (oligophagous), was compared. The influence of seasonal changes in plants as food for both insects was examined, in particular, the effects of nitrogen and sorbitol in leaves. In the laboratory, Y. evonymellus accepts Crataegus monogyna, a host plant of Y. padellus, and Y. padellus accepts Prunus padus, the host plant of Y. evonymellus. P. padus is the most suitable food plant for Y. evonymellus. No difference in food-quality for Y. padellus was found between C. monogyna and P. padus. The performance of both species on P. padus is less influenced by seasonal changes than on Crataegus. The suitability of Crataegus decreases during the season. This is probably caused by the decrease of its nitrogen content, and not by the decrease of sorbitol in the plant. The monophagous, Y. evonymellus, is more sensitive to seasonal changes in its food when fed with a non host plant than the oligophagous Y. padellus. In oviposition experiments both species have a preference for their normal host-plants.     

Host associations of <Emphasis Type="Italic">Coenonympha hero</Emphasis> (Lepidoptera: Nymphalidae) in northern Europe: microhabitat rather than plant species

Understanding ecological requirements of endangered species is a primary precondition of successful conservation practice. Regrettably, we know surprisingly little about the life history of numerous threatened insects, and about their use of larval host plants in particular. The brown butterflies (Nymphalidae: Satyrinae) have traditionally been considered polyphagous on grasses and indiscriminatory in their oviposition behavior. However, detailed studies on several species have revealed local specialization in host plant use as well as the decisive role of microlimatic conditions as determinants of habitat quality. The present study addresses host plant relationships in the endangered brown butterfly Coenonympha hero (L.) at the northern limit of its European distribution. We combine laboratory-based host preference and performance tests with an analysis of microhabitat use by adult butterflies in the field. Both lines of evidence suggest that C. hero is polyphagous enough not to be associated with one particular host species. Oviposition choices of C. hero are not driven by host plant species but rather by structural characteristics of the substrate. The preferred rigid needle-like structures may serve as cues of ‘transparent’ vegetation which allows the larvae to benefit from sunlight reaching the lower strata of the tuft. Our results suggest that conservation efforts should prioritize microclimatic parameters, rather than the presence of any particular host plant species, as decisive determinants of habitat quality in C. hero.     

Plant scents modify innate colour preference in foraging swallowtail butterflies

Flower-visiting insects exhibit innate preferences for particular colours. A previous study demonstrated that naive Papilio xuthus females prefer yellow and red, whereas males are more attracted to blue. Here, we demonstrate that the innate colour preference can be modified by olfactory stimuli in a sexually dimorphic manner. Naive P. xuthus were presented with four coloured discs: blue, green, yellow and red. The innate colour preference (i.e. the colour first landed on) of the majority of individuals was blue. When scent from essential oils of either orange flower or lily was introduced to the room, females’ tendency to select the red disc increased. Scents of lavender and flowering potted Hibiscus rosa-sinensis, however, were less effective. Interestingly, the odour of the non-flowering larval host plant, Citrus unshiu, shifted the preference to green in females. In males, however, all plant scents were less effective than in females, such that blue was always the most favoured colour. These observations indicate that interactions between visual and olfactory cues play a more prominent role in females.     

Conditioning as a factor in parasitoid host plant preference

The relative effects of larval and adult conditioning on Diglyphus isaea host plant preference and subsequent parasitism were investigated. Parasitoid larvae were reared on Chromatomyia syngenesiae on lettuce, chrysanthemum or in isolation, and female parasitoids were exposed to hosts on either lettuce or chrysanthemum. Hosts on lettuce and chrysanthemum were then presented to assess parasitoid preference. Larval and adult D. isaea conditioning only slightly affected the females selection of host plant type on which the host larvae were located. The major effect of conditioning was a reduction in the number of eggs laid after larvae and adults were conditioned on chrysanthemum and particularly when both stages were conditioned on this host plant.     

The roles of adult and larval specialisations in limiting the occurrence of five species of Dacus (Diptera: tephritidae) in cultivated fruits

Summary The relative importance of adult preferences or specialisations of larval physiology in restricting the host range of five species of Dacine fruit flies (Diptera: Tephritidae) was examined, with particular emphasis on their utilization of cultivated fruits. The species; D. tryoni, D. jarvisi, D. cucumis, D. musae and D. cacuminatus differ widely in host range with D. tryoni being highly polyphagous while D. cacuminatus is virtually monophagous. Laboratory experiments showed that larvae of all species survived and developed in many cultivated fruits in which the specialists never occur in the field. By contrast the oviposition preferences and specificity of adult females differed widely between species. Female D. tryoni oviposited in most species of fruit. The specialised species; D. cucumis, D. musae and D. cacuminatus strongly preferred their usual hosts and would not oviposit in novel fruits even in the absence of the preferred host. In contrast, D. jarvisi consistently preferred its main native host but when this was not offered readily accepted cultivated fruits. These differences in preference are consistent with the pattern of infestation displayed by each species in the field. The study indicate that, in general, the occurrence of these species of Dacus in cultivated fruits is constrained more by the behavioural preferences of adult females than by larval specialisations. A genetic change in some aspect of host recognition or acceptance would be necessary for the specialised species to regularly infest cultivated fruits though no change in larval characteristics may be needed. As the types and concentrations of defensive secondary compounds may differ between native and cultivated fruits this conclusion cannot be extended to host shifts among native fruits.