Papilio aegeus Donovan (Lepidoptera: Papilionidae) host plant range evaluated experimentally on ancient angiosperms

Abstract  Chemical similarities among ancient Angiosperms presumably played a role in the ecological and evolutionary diversification of the swallowtail butterflies (Papilionidae). The abilities of neonate larvae of the Citrus swallowtail, Papilio (= Princeps ) aegeus (from Queensland, Australia), to eat, survive and grow on leaves (a choice of young and old) of 34 plant species from families of ancient Angiosperms; 8 Rutaceae, 3 Magnoliaceae, 13 Lauraceae, 3 Monimiaceae, 1 Aristolochiaceae, 2 Apiaceae, 1 Sapotaceae, 1 Winteraceae and 2 Annonaceae were tested. It was apparent that there is genetic variation in populations of Rutaceae-specialised Australian P. aegeus for acceptance, consumption and larval growth, reflecting differential suitability of some native Australian Lauraceae species as food plants (as well as certain Winteraceae, Monimiaceae and non-Australian Magnoliaceae, Lauraceae and Annonaceae). No consumption or survival of P. aegeus was seen on Aristolochia elegans (Aristolochiaceae) or Pouteria australis (Sapotaceae) despite literature records alluding to this possibility. The Rutaceae specialist P. aegeus appears to have the fundamental detoxification capabilities for processing many existing species of the basal Angiosperm families, without having direct ancestors that historically had fed on them.     

Aristolochiaceae‐ and Asteraceae‐feeding by larvae of Papilio xuthus L. (Lepidoptera: Papilionidae) in Japan: A review

Our recent observations of Aristolochiaceae‐ and Asteraceae‐feeding by larvae of Papilio xuthus L. (Lepidoptera: Papilionidae), which is generally a typical Rutaceae‐feeding swallowtail, inspired us to survey published works describing its host range and aspects of its chemical ecology. Papilio xuthus larvae have been observed feeding on a total of 22 plant species other than members of Rutaceae, including those of Asarum (Aristolochiaceae) and Cosmos (Asteraceae). Most observation records and our current study indicated that Aristolochiaceae‐feeding by P. xuthus larvae was not due to oviposition error, but to larval movement to Asarum from adjacent rutaceous hosts after they had become unsustaining. Many larvae developed on Asarum to further stadia but we confirmed that some did not, indicating that Asarum was unsuitable for some individuals. According to previous and current observations, P. xuthus females oviposit directly on Cosmos and their larvae can develop to adults although, again, their performance on these plants is not always favorable. Host choice by swallowtail butterflies is determined both at the egg‐laying and larval‐feeding stages. Although adult P. xuthus use a mixture of unique secondary metabolites as their host‐location cue, larvae use primary nutrients as their major phagostimulants. Larval feeding on Asarum could suggest a reversion triggered by vestigial chemosensitivity to ancestral olfactory and/or gustatory cues, because several major clades of Papilionidae feed on Aristolochiaceae. Further studies on the phytochemical/chemosensory bases for these associations are needed if we are to understand the evolutionary pathway of host selection in P. xuthus, as indicated by these relatively unusual host‐seeking behaviors.     

Interactions between Papilionidae and ancient Australian Angiosperms: evolutionary specialization or ecological monophagy?

The evolution of host range for insect herbivores involves many behavioral, physiological, and biochemical adaptations that often lead to locally specialized populations or species. Such specialization may be constrained by ecological factors (e.g., local host availability) or by evolutionary factors (e.g., phylogenetic divergence in behavioral, physiological, or biochemical detoxification enzymes; and potential inabilities to return to ancestral hosts). While insect adaptations to new hosts can be rapid, ancient detoxification systems may persist in some lineages of swallowtail butterflies (Papilionidae) for millions of years. Here, we test various species of specialized species/populations of Papilionidae (Lepidoptera) from North America and from Australia on an array of Australian host plant families in order to determine whether the current feeding constraints reflect loss of capabilities to recognize and use hosts other than their current (local) favorites. We selected two species of Lauraceae specialists (Papilio troilus L. and Papilio palamedes Drury) from North America and one locally specialized population of Papilio glaucus L. that only uses one plant species in the Magnoliaceae in Florida. We also examined three species/populations of Australian swallowtails for comparison, including the Monimiaceae‐specialized Graphium macleayanum moggana L. E. Couchman, the Rutaceae‐specialized Papilio aegeus Donovan, and the Annonaceae‐specialized Graphium eurypylus L. Our aim was to determine whether neonate larvae of these six specialists could survive on any plants other than their currently favored species. While the Lauraceae specialists could use nothing else and were thus evolutionarily constrained, the Magnoliaceae‐, Rutaceae‐, and Monimiaceae specialists all had common abilities to accept, feed, and grow on plants in the Lauraceae, Monimiaceae, Magnoliaceae, and Rutaceae families. Even the Annonaceae specialist was discovered using Magnoliaceae in the field, suggesting existence here also of both flexiblity in preferences and detoxification abilities and ‘ecological monophagy’.     

Ecological monophagy in Tasmanian Graphium macleayanum moggana with evolutionary reflections of ancient angiosperm hosts

Local host plant specialization in an insect herbivore may be caused by numerous factors, including host-specific natural enemy pressures or a local lack of suitable host-plant choices that are available elsewhere in its range. Such local specialization or ＂ecological monophagy＇, for whatever reason, may reflect reduced ability to behaviourally accept or physiologically utilize other allopatric hosts that are naturally used elsewhere by the species. We tested this feeding specialization hypothesis using the Tasmanian subspecies of Macleay＇s swallowtail butterfly, Graphium macleayanum moggana （Papilionidae）, which uses only a single host-plant species, Antherosperma moschatum （southern sassafras, of the Monlmiaceae）. Further north, this same butterfly species （G. m. macleayanum） uses at least 13 host-plant species from seven genera and four families （Lauraceae, Rutaceae, Winteraceae, and Monlmiaceae）. Our larval feeding assays with G. m. moggana from Tasmania showed that certain Magnoliaceae and Lauraceae could support some larval growth to pupation. However, such growth was slower and survival was lower than observed on their normal southern sassafras host （Monimiaceae）. We also found that toxicity of particular plant species varied tremendously within plant families （for both the Magnoliceae and the Monlmiaceae）.     

Mechanisms and consequences of selective oviposition by the zebra swallowtail butterfly

Zebra swallowtail butterflies, Eurytides marcellus, were studied in the field to determine (1) whether the behavioural response of a female to host plant individuals, pawpaws (Asimina spp.), correlated with characteristics of the plant foliage, (2) whether selective oviposition improved larval survivorship, and (3) how unpredictable plant qualities affected the translation of female choice into larval success. Females laid eggs preferentially on pawpaws bearing the youngest leaves, while non-hosts and pawpaws bearing mostly mature leaves were rejected before or after the females touched the plant. By rejecting unsuitable plants early in evaluation, females concentrated their time and risk on the plants most likely to provide an oviposition site. Larvae survived longer on oviposition plants than on plants that were rejected, but unpredictable components of plant quality, particularly predation on larvae, could weaken the correlation.     

Integrating ancient patterns and current dynamics of insect–plant interactions: Taxonomic and geographic variation in herbivore specialization

Abstract The search for pattern in the ecology and evolutionary biology of insect–plant associations has fascinated biologists for centuries. High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted. This review addresses several aspects of local insect specialization, host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence, and ecological (including “hybrid”) speciation, with special reference to the generation of biodiversity and the geographic and taxonomic identification of “species borders” for swallowtail butterflies (Papilionidae). From ancient phytochemically defined angiosperm affiliations that trace back millions of years to recent and very local specialized populations, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of localized ecological patterns and genetically based evolutionary processes. They have served as a useful group for evaluating the feeding specialization/physiological efficiency hypothesis. They have shown how the abiotic (thermal) environment interacts with host nutrirional suitability to generate “voltinism/suitability” gradients in specialization or preference latitudinally, and geographical mosaics locally. Several studies reviewed here suggest strongly that the oscillation hypothesis for speciation does have considerable merit, but at the same time, some species-level host specializations may lead to evolutionary dead-ends, especially with rapid environmental/habitat changes involving their host plants. Latitudinal gradients in species richness and degree of herbivore feeding specialization have been impacted by recent developments in ecological genetics and evolutionary ecology. Localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious, with simple definitions still debated. However, molecular analyses combined with ecological, ethological and physiological studies, have already begun to unveil some answers for many important ecological/evolutionary questions.     

Tyramine from the leaves of wild parsnip: a stimulant and synergist for oviposition by the black swallowtail butterfly

Abstract .Oviposition stimulants from the foliage of wild parsnip, Pastinaca sativa (Apiaceae), were isolated by column chromatography and HPLC and tested in bioassay experiments with hand-held female black swallowtail butterflies, Papilio polyxenes (Lepidoptera: Papilionidae). Two of the stimulants were identified as tyramine and trans -chlorogenic acid. A combination of tyramine, trans -chlorogenic acid and an active neutral fraction was needed to elicit a significant oviposition response. These results are discussed in the context of previous research on the oviposition stimulants of swallowtail butterflies and on the significance of tyramine as a neuromodulator of physiological processes in invertebrates.     

Evolutionary conservatism of oviposition preference in a widespread polyphagous insect herbivore, Papilio zelicaon

We analyzed geographic differentiation in oviposition preference in the anise swallowtail butterfly, Papilio zelicaon Lucas, which is one of the most widely distributed and polyphagous butterflies in western North America. Among 13 populations that span 1200 km of the range of P. zelicaon in the Pacific Northwest of North America, the overall oviposition preference hierarchy has not diverged significantly, even though these populations differ in the plant species they use in the field. The results indicate that differences in host availability and use have not favored major reorganizations in the preference hierarchy of ovipositing females. Instead, this butterfly has a conserved preference hierarchy that varies within a narrow range among populations. All populations ranked the four test plant species in the same overall relative order, even though these populations differ in the plant species they use in the field. Received: 9 February 1996 / Accepted: 24 February 1997     

Leaf buds, a factor in host selection by Battus philenor butterflies

ABSTRACT.

• 1 Field and laboratory experiments identified a character intrinsic to Aristolochia reticulata Nutt. host plants, the terminal leaf bud, that is involved in host-selection behaviour by female pipevine swallowtail butterflies (Battus philenor L.) searching for oviposition sites.
• 2 In the field, the frequency with which females landed on non-host buds declined seasonally as the proportion of host foliage that consisted of buds decreased. Female butterflies did not land on non-host species in proportion to their abundance; rather, females landed on those non-host species whose buds resembled those of A.reticulata.
• 3 A.reticulata plants whose terminal leaf bud was concealed by plastic tape were less susceptible to oviposition in the field than were control plants.
• 4 Female butterflies released in a large, outdoor enclosure were conditioned to search for leaf buds only when exposed to a host species bearing a prominent terminal leaf bud.
• 5 The significance of conditioning of leaf-bud searching behaviour is discussed with respect to discrimination between hosts and non-hosts, between host species, and among plants within a host species.

     

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     

The effect of host plant on larval survivorship of the Alaskan swallowtail butterfly (Papilio machaon aliaska)

The Alaskan swallowtail butterfly, Papilio machaon aliaska (Lepidoptera: Papilionidae), uses three plant species as host plants. Cnidium cnidiifolium (Turcz.) Schischk. belongs to the family Apiaceae, the ancestral host‐plant family of the P. machaon group. Artemisia arctica Less. and Petasites frigidus (L.) Franch, in contrast, belong to the distantly related Asteraceae family and were colonized relatively recently by this group of butterflies. Previous work has shown that larval survival is highest on the novel host plants when natural enemies are present in the field. Here I examine whether P. m. aliaska fitness varied when individuals were reared on the three host plants in a common environment, free of environmental and ecological complications such as predation. I collected 12 P. m. aliaska females and measured their reproductive success when their progeny were reared on each of the three host plants. I assessed larval fitness on each of the hosts by recording the percentage pupation and percentage emergence as well as by measuring pupal mass. I found that larvae reared on the ancestral host plant, C. cnidiifolium, had higher fitness than did larvae reared on either of the novel host plants, A. arctica or P. frigidus. Larvae reared on C. cnidiifolium were more likely to pupate, achieved a greater pupal mass, and had higher emergence rates than larvae reared on the novel hosts. I interpret these results to mean that, in the absence of predation, the ancestral host plant is a better host for P. m. aliaska larvae than either novel host and I contend that this result does not appear to support the hypothesis that P. m. aliaska populations in central Alaska are divided into host races.     

Patch dynamics ofGlaucopsyche lygdamus (Lycaenidae): correlations between butterfly density and host species diversity

Glaucopsyche lygdamus egg densities were surveyed over a 2000-m section of Gold Creek and at 30 different isolated patches in the Gold Basin drainage in Colorado. Host plant numbers and diversity were quantified, as well as other variables potentially influencing butterfly population size, such as patch size and isolation. Egg densities correlated significantly only with measures of host species diversity. Patches consisting of a single host species, no matter how large, did not support high butterfly densities, but patches of multiple, equitably distributed host species did. The most likely explantation, in light of oviposition preference and larval performance data accumulated for this butterfly species, is that host species diversity is necessary for the persistence ofG. lygdamus populations, because alternative host species buffer population losses during poor or unusual years. The dependence of both ovipositing butterflies and developing larvae on the ephemeral, young, host plant flowers make the butterfly especially vulnerable to year-to-year variation in host plant availability and quality.     

Positive effects of cyanogenic glycosides in food plants on larval development of the common blue butterfly

Cyanogenesis is a widespread chemical defence mechanism in plants against herbivory. However, some specialised herbivores overcome this protection by different behavioural or metabolic mechanisms. In the present study, we investigated the effect of presence or absence of cyanogenic glycosides in birdsfoot trefoil (Lotus corniculatus, Fabaceae) on oviposition behaviour, larval preference, larval development, adult weight and nectar preference of the common blue butterfly (Polyommatus icarus, Lycaenidae). For oviposition behaviour there was a female-specific reaction to cyanogenic glycoside content; i.e. some females preferred to oviposit on cyanogenic over acyanogenic plants, while other females behaved in the opposite way. Freshly hatched larvae did not discriminate between the two plant morphs. Since the two plant morphs differed not only in their content of cyanogenic glycoside, but also in N and water content, we expected these differences to affect larval growth. Contrary to our expectations, larvae feeding on cyanogenic plants showed a faster development and stronger weight gain than larvae feeding on acyanogenic plants. Furthermore, female genotype affected development time, larval and pupal weight of the common blue butterfly. However, most effects detected in the larval phase disappeared for adult weight, indicating compensatory feeding of larvae. Adult butterflies reared on the two cyanogenic glycoside plant morphs did not differ in their nectar preference. But a gender-specific effect was found, where females preferred amino acid-rich nectar while males did not discriminate between the two nectar mimics. The presented results indicate that larvae of the common blue butterfly can metabolise the surplus of N in cyanogenic plants for growth. Additionally, the female-specific behaviour to oviposit preferably on cyanogenic or acyanogenic plant morphs and the female-genotype-specific responses in life history traits indicate the genetic flexibility of this butterfly species and its potential for local adaptation.     

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.     

外来植食性广聚萤叶甲对非靶标植物的潜在影响

为评估以入侵豚草为食的外来广聚萤叶甲（Ophraella communa）对非靶标植物的潜在生态风险,采用选择性试验测定了广聚萤叶甲成虫和幼虫对当地代表性植物的取食选择,观察了幼虫在选出的植物上生长发育的适合度表现。结果表明：在5大类52种测试植物中,广聚萤叶甲成虫和幼虫不同程度地取食向日葵、苍耳、天明精、菊芋（仅成虫）、紫茎泽兰（仅幼虫）和石胡荽（仅幼虫）;野外罩笼非选择性测定发现,初孵幼虫在苍耳和向日葵8个品种上可完成发育,直到成虫产卵,并观察到在菊芋上完成幼虫发育,个别到成虫但未产卵;在这些植物上幼虫存活率明显降低,蛹质量明显减轻,成虫产卵明显减少。本文还分析了广聚萤叶甲对少数本土植物以及经济作物向日葵的潜在生态风险。     

How discriminating are cabbage butterflies?

The egg-laying responses of cabbage butterflies Pieris rapae L. to differences in the size, quality and spatial distribution of available oviposition sites, were studied in the laboratory (Australia) and the field (Australia and Canada). Differences on three scales were investigated: between leaves within the same plant, between plants within a patch, and between patches of plants. The butterflies lay most eggs on the larger, older leaves of plants, though the oldest are sometimes avoided. Larger plants also receive more eggs than smaller ones of the same cultivar, but cultivar preferences may override the response to size. The butterflies do not discriminate against plants already bearing eggs or larvae, unless larval feeding damage to the plant is severe. They lay more eggs on young plants than old ones of the same size; plants grown in the lower of two light intensities also received more eggs. Australian butterflies discriminate not only between different species of crucifers, but also between varieties of the same species. This discrimination against less acceptable varieties is just as strong when plants of preferred varieties are not present, as when both varieties occur in the same patch. The observed responses are discussed in relation to the butterflies’ host-finding behaviour and the adaptive significance of the lack of a response to eggs and larvae is considered.     

HOST-PLANT RELATIONSHIPS IN THE PAPILIONIDAE (LEPIDOPTERA): PARALLEL CLADOGENESIS OR COLONIZATION?

Abstract— Stepwise coevolution, as defined by Ehrlich and Raven (1964) and others, can be equated with parallel cladogenesis or association by descent (Mitter and Brooks, 1983). I review the insect/plant literature and discuss recent cladistic findings for the Papilionidae, and compare two contrasting theories: 1) that insect/host associations have evolved through parallel cladogenesis; or 2) that insects have 'colonized' their hosts subsequent to plant cladogenesis. I conclude that no documented examples of parallel cladogenesis between insects and plants are known. The swallowtail cladograms instead offer evidence in support of the second theory. They suggest that host association patterns in the Papilionidae have resulted from repeated colonization of plants belonging to a relatively small number of families. I discuss data which indicate that plant secondary chemicals have been important 'barriers' to colonization ( sensu Ehrlich and Raven, 1964), and have in large part mediated host switching in the Papilionidae.     

Host plant utilization by butterfly larvae in the Andaman and Nicobar Islands (Indian Ocean)

The larval food plants of the butterflies of the Andaman and Nicobar islands have not been studied, although the butterfly fauna per se is fairly well known. For the first time we report the food plants of the larvae of 120 species of butterflies from these islands on the basis of laboratory rearing and field studies. This information is essential for the formulation of management programmes for butterfly conservation on these islands which are known to harbour critical swallowtail and (possibly) danaine faunas.     

Experimental evidence of host race formation in Mitoura butterflies (Lepidoptera: Lycaenidae)

A population of herbivorous insects that shifts to a novel host can experience selection pressures that result in adaptation to the new resource. Host race formation, considered an early stage of the speciation process, may result. The current study investigates host shifts and variation in traits potentially involved in the evolution of reproductive isolation among populations of the juniper hairstreak butterfly, Mitoura gryneus. Mitoura are closely associated with their host trees (Cupressaceae) and exhibit host plant fidelity: in addition to larval development and oviposition, host trees support male leks and mating. Female oviposition preference for the natal host, and differential fitness of larvae when reared on natal versus alternate hosts, are indications that specialization and local adaptation to the natal host plant are occurring. Populations with single host plant associations (Juniperus ashei, J. pinchotii and J. virginiana) as well as populations with multiple hosts (both J. ashei and J. pinchotii) were examined. Concordance between female preference and larval performance was found for J. ashei‐associated populations. Population‐level variation in the patterns of female preference and larval performance, both within and among host associations, may reflect differences in the timing and direction of colonization of hosts. For a single nominal species that otherwise exhibits no morphological or phenological differences, the experimental assessment of specialization and host fidelity in M. gryneus provides strong support for the hypothesis of ongoing host race formation in these butterflies.