Battus Philenor Research Articles

Aggregative feeding of pipevine swallowtail larvae enhances hostplant suitability.

Many hypotheses have been proposed to explain the adaptive significance of aggregative feeding in the Lepidoptera. One hypothesis that has received little attention is how induced plant responses may be influenced by aggregative feeding, as compared to feeding by solitary larvae. This study investigated the role of aggregative feeding of the pipevine swallowtail, Battus philenor, in California with special emphasis on the induced responses to herbivory of its hostplant. Here, I show that first-instar larvae develop faster when feeding in a large aggregation compared to solitary or small groups of larvae. Furthermore, I show that this effect is mediated by a larval-density-dependent response in the plant and is independent of prior larval experience and direct interaction among larvae. These results indicate that large groups of larvae can effectively enhance hostplant suitability. A separate experiment showed that larvae feeding on previously damaged leaves had a reduced growth rate. Thus, following initial damage a plant first goes through a period of increased suitability, followed by induced resistance against subsequent herbivory. Aggregative feeding in this system may be an adaptive strategy for larvae to manipulate hostplant suitability, adding a new dimension to the role of aggregative feeding for the Lepidoptera.

ANOTHER PERSPECTIVE ON THE SLOW-GROWTH/HIGH-MORTALITY HYPOTHESIS: CHILLING EFFECTS ON SWALLOWTAIL LARVAE

The slower-growth/higher-mortality hypothesis proposes that reduced herbivore growth rates benefit plants because slower growing herbivores remain vulnerable to predator attack for an extended time period, resulting in a lower reduction in plant fitness attributed to herbivory. We propose cooling events as an alternative mechanism leading to higher mortality for slower growing larvae. We observed that, in the absence of predators, slower growing pipevine swallowtail (Battus philenor) larvae had higher mortality compared to faster growing larvae during the unseasonably cool spring temperatures of 1998. However, this was not true for the warmer spring of 1999. Laboratory experiments showed that the probability of surviving a chill coma increased with larval mass. We propose that smaller larvae are susceptible to chilling events because they have less energy reserved for metabolism during a chill coma, and that “warm” chill events near the activity threshold may be more lethal than “cold” chill events. Weather station data since 1951 and field data collected from 1976 to 2000 suggest that exposure to chill events below the chill coma threshold is not uncommon for these larvae. We propose that faster growth may be important for larvae because slower growing larvae remain at a chill-susceptible size for an extended period of time. Corresponding Author: S. J. Simpson.

Chemical defence ofBattus philenorlarvae against attack by the parasitoidTrogus pennator

Abstract1. Parasitoids in the genusTrogus(Hymenoptera: Ichneumonidae) attack the larvae of swallowtail butterflies (Lepidoptera: Papilionidae). Only two of the three major tribes of the subfamily Papilioninae are attacked although species of all three tribes commonly occur together. The tribe Troidini is relatively free of parasitoids of any kind, and it has been proposed that the aristolochic acids sequestered by troidines protect them from parasitism.2. The responses ofT. pennator(Fabricius) to the sympatric troidineBattus philenor(Linnaeus) were examined. Three hypotheses that could explain why this wasp does not parasitiseB. philenorwere considered. (1)Battus philenordoes not produce compounds used by the wasp to locate hosts. (2) The larval integument contains compounds that deter attack. (3) The parasitoid offspring cannot survive inB. philenor.3. The first hypothesis was not supported as the frass ofB. philenorlarvae was found to act as a searching arrestant comparable to the frass of a host species.4. The second hypothesis was supported. TheB. philenorlarvae were rejected when the wasps examined them using their antennae, and ethanolic washes ofB. philenorcuticle deterred attack byT. pennatorwhen applied to otherwise acceptable host larvae. Bioassays of fractions of the ethanolic wash and of pure aristolochic acids established that aristolochic acids were at least partly responsible for the deterrent effect.5. The third hypothesis was also supported. Larvae ofB. philenorattacked by the parasitoids developed into butterflies.6. These results indicate that both behavioural and physiological barriers, the former attributable at least in part to sequestered compounds and the latter of unknown mechanism, preventT. pennatorfrom parasitisingB. philenor.

The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor

Summary The California population of the pipevine swallowtail Battus philenor is a specialist on the Dutchman’s pipe Aristolochia californica, an endemic vine that is densely covered with trichomes. Populations of B. philenor outside California use other Aristolochia species that are largely glabrous. The average clutch size of the pipevine swallowtail is larger in California compared with populations elsewhere and larvae feed gregariously until late in the third instar. In the field, caterpillars consumed more leaf material and showed preference for portions of leaves with trichomes removed. However, large groups of caterpillars were consistently observed feeding on the apical portion of the plant, where trichome density was highest. Smaller groups of caterpillars were observed feeding more often on mature leaves on the lower portions of the plant, where trichome density was lower. Laboratory experiments showed that the walking speed of a commonly observed predator, larvae of the green lacewing Chrysopa carnea, was reduced as trichome density increased. Furthermore, lacewing search efficiency and capture rate of a model prey item were compromised by high trichome density. In an additional field experiment, no difference was found in the percentage mortality of groups of four and 12 caterpillars. However, growth rate of the larger group was accelerated by 25% compared with smaller groups. In an experiment using a ladybird beetle larva Hippodamia convergens as the predator, no difference was observed in absolute mortality of caterpillars, suggesting that group size does not function directly as a defence against predators. First instar caterpillars are most vulnerable to predators, thus feeding in larger groups may benefit caterpillars by accelerating growth. Feeding in large groups may also be an effective strategy for B. philenor to overcome plant trichomes and feed on portions of the plant conducive to faster development. However, feeding on areas with dense trichomes does not appear to provide larvae with a refuge from predators.

The lethal plant defense paradox remains: inducible host‐plant aristolochic acids and the growth and defense of the pipevine swallowtail

AbstractToxic plants with sequestering specialists are presented with a problem because plant derived toxins protect herbivores against natural enemies. It has been suggested that early induction of toxins and later relaxation of these defenses may help the plant resolve this problem because neonate caterpillars incur the physiological cost of dealing with toxins in early life, but are denied toxins when they are able to sequester them efficiently. In California, the pipevine swallowtail, Battus philenor L. (Lepidoptera: Papilionidae), feed exclusively on Aristolochia californica Torrey (Aristolochiaceae), an endemic vine that contains toxic alkaloids called aristolochic acids that caterpillars sequester to provide chemical defense in immature and adult stages. In a field experiment, the concentration of aristolochic acids doubled in the plant following leaf damage and returned to constitutive levels after six days. Neonate pipevine swallowtail caterpillars showed no aversion to high levels of aristolochic acid in a preference test. Caterpillars reared on leaves with supplemented aristolochic acid showed no physiological cost or increased mortality compared to caterpillars reared on un‐supplemented leaves. Searching efficiency and capture rate of lacewing larvae (Chrysoperla), a common predator of first instar caterpillars, was compromised significantly after feeding on caterpillars reared on leaves with supplemented concentrations of aristolochic acid compared to caterpillars feeding on control plants. Additionally, mortality of lacewings increased when they were provided with a diet of B. philenor caterpillars reared on supplemented leaves compared to caterpillars reared on control leaves. Thus, the induction of aristolochic acids in the plant following leaf damage does not resolve the problem confronted by the plant and may confer benefits to this sequestering specialist.

Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L.): evidence and ecological implications

It has long been assumed that the North American pipevine swallowtail, Battus philenor (L.) (Papilionidae, Troidini), is protected from natural enemies by aristolochic acids sequestered from its Aristolochia food plants. This study confirmed that populations of B. philenor from Virginia and east Texas sequester these compounds. A comparison of the aristolochic acid profiles of the Virginia butterflies and their A. macrophylla food plants revealed several differences. The aristolochic acid fraction of the foliage was dominated by aristolochic acids I and II, whereas the insects had a much lower proportion of aristolochic acid II and contained, in addition, substantial amounts of aristolochic acids Ia and IVa, which were not detected in the plants. The eggs, larval integument, osmeterial glands, pupal cuticle, and adults (wings and bodies) all contained aristolochic acids. These findings help explain the abundant ecological data indicating that both immature and adult B. philenor are unpalatable and protected from natural enemies.

The molecular basis of melanism and mimicry in a swallowtail butterfly.

Melanism in Lepidoptera, either industrial or in mimicry, is one of the most commonly cited examples of natural selection [1] [2]. Despite extensive studies of the frequency and maintenance of melanic genes in insect populations [1] [2], there has been little work on the underlying molecular mechanisms. Nowhere is butterfly melanism more striking than in the Eastern Tiger Swallowtail (Papilio glaucus) of North America [3] [4] [5]. In this species, females can be either yellow (wild type) or black (melanic). The melanic form is a Batesian mimic of the distasteful Pipevine Swallowtail (Battus philenor), which is also black in overall color. Melanism in P. glaucus is controlled by a single Y-linked (female) black gene [6]. Melanic females, therefore, always have melanic daughters. Black melanin replaces the background yellow in melanic females. Here, we show that the key enzyme involved is N-beta-alanyl-dopamine-synthase (BAS), which shunts dopamine from the melanin pathway into the production of the yellow color pigment papiliochrome and also provides products for cuticle sclerotization. In melanic females, this enzyme is suppressed, leading to abnormal melanization of a formerly yellow area, and wing scale maturation is also delayed in the same area. This raises the possibility that either reduced BAS activity itself is preventing scale sclerotization (maturation) or, in contrast, that the delay in scale maturation precludes expression of BAS at the correct stage. Together, these data show how changes in expression of a single gene product could result in multiple wing color phenotypes. The implications for the genetic control of mimicry in other Lepidoptera are discussed.

A Model Without a Mimic: Aristolochic Acids from the California Pipevine Swallowtail, Battus philenor hirsuta, and Its Host Plant, Aristolochia californica

The pipevine swallowtail, Battus philenor, feeds exclusively on plants in the genus Aristolochia, many of which are known to contain the toxic alkaloids collectively known as aristolochic acids. Pipevine swallowtails sequester these compounds and use them for their own defense against predators. Numerous palatable butterflies are involved in Batesian mimicry complexes with B. philenor over its range. The California subspecies of the pipevine swallowtail, B. philenor hirsuta, has no mimics. Analysis of the butterfly and its only host plant, Aristolochia californica, indicate that both contain aristolochic acid. Aristolochic acid (I) and (II) are the primary aristolochic acids found in A. californica. The highest concentration of aristolochic acids was found in the flowers, which bloom before B. philenor emerges. Concentrations of aristolochic acids decreased in the leaves but not in stem tissue over the course of the season. Butterflies contained primarily aristolochic acid (I). Aristolochic acid content of individuals from Arizona, which are involved in mimicry complexes, did not differ from California populations. Thus, lack of California mimics cannot be attributed to low aristolochic acid content of the model.

Feeding Experience Enhances Attraction of Female Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae) to Food Plant Odors

Learning in insects is broadly defined as a temporary modification of behavioral responsiveness as a result of experience (Papaj and Prokopy, 1989). According to Papaj and Prokopy (1989) and Thorpe (1993), a decline in a response in the absence of continued experience is another criterion that can be used to specify learning in insects. Learning in phytophagous insects may be manifested as altered responses to host plants following some type of experience. Individual insects exposed to different foods tend to select the food they most recently accepted and experienced, compared to novel foods (Papaj and Prokopy, 1989). Previous experience with a plant or its odor affects the behavior of many adult insects, such as Battus philenor (L.) (Papaj, 1986a,b), Leptinotarsa decemlineata (Say) (Visser and Thiery, 1986), and Trichoplusia ni (Hubner) (Landolt and Molina, 1996). In the pipevine swallowtail butterfly B. philenor, the positive effect of exposure to one food plant species on food acceptance was reversed by exposure to a second food plant species (Papaj et al., 1986a). Diaprepes abbreviatus is a polyphagous insect that feeds on foliage of at least 76 plant species (Martorell, 1976). The weevils are attracted to odors of food plants (Beavers et al., 1982; Harari and Landolt, 1997) and form aggregations on or near new growth of host trees (Beavers et al., 1982). Aggregations

Innate colour preferences and flexible colour learning in the pipevine swallowtail

The importance of innate preferences and learned associations in choice of flower colours were investigated for the pipevine swallowtail butterfly,Battus philenor(Papilionidae). Naive butterflies showed innate colour preferences for yellow and, to a lesser extent, blue and purple. Apart from their innate preferences, they were able to learn within 10 flower visits to associate floral colour with the presence of nectar rewards in yellow or magentaLantana camara(Verbenaceae) flowers. Continued experience resulted in greater discrimination in favour of the rewarding colour. Most individuals readily shifted their foraging behaviour when the colour of the rewarding flower was changed. A capacity for rapid and flexible associative learning presumably allows butterflies to adjust their foraging efforts in response to floral rewards that vary over space or time. 1997 The Association for the Study of Animal Behaviour

Learning of leaf shape by pipevine swallowtail butterflies: A test using artificial leaf models

Learning of leaf shape by pipevine swallowtail butterflies: A test using artificial leaf models

Female-limited variability in mimicry in the swallowtail butterfly Papilio polyxenes Fabr.

Variation in dorsal and ventral aspects of mimetic wing patterns was measured in the sexually dimorphic swallowtail butterfly Papilio polyxenes, a Batesian mimic of Battus philenor. The pattern on the dorsal surface of the wings makes females better mimics than males and was more variable in females. The pattern on the ventral surface of the hind wings, which provides a similar degree of mimicry in both sexes, was equally variable in both sexes. Full-sib ANOVA indicated that variability in dorsal and ventral patterns was similarily heritable in both sexes, suggesting that the increased variability in females is not simply the result of suppressed expression of genetic variation in males. The results are consistent with the hypothesis that variation in two sets of modifier loci, only one of which is expressed in males, influences the dorsal pattern, resulting in greater variability in females. The nonmimetic dorsal pattern in males is probably maintained as a consequence of sexual selection arising from male-male competition in territorial encounters. The generality of the reduced male variability in the Lepidoptera is discussed.

Sequestration of plant secondary compounds by butterflies and moths

A number of aposematic butterfly and moth species sequester toxic substances from their host plants. Some of these insects can detect the toxic compounds during food assessment. Some pipevine swallowtails use aristolochic acids among the host finding cues during oviposition and larval feeding and accumulate the toxins in the body tissues throughout all life stages. Likewise, a danaine butterfly,Idea leuconoe, which sequesters high concentrations of pyrrolizidine alkaloids in the body, lays eggs in response to the specific alkaloid components contained in the apocynad host. Insect species sharing the same poisonous host plants may differ in the degree of sequestration of toxins. Two closely ralated aposematic geometrid moth species,Arichanna gaschkevitchii andA. melanaria, sequester a series of highly toxic diterpenoids (grayanotoxins) in different degrees, while a cryptic geometrid species,Biston robstus, does not sequester the toxins, illustrating the diversity in adaptation mechanisms even within the same subfamily. By contrast, a number of lepidopteran species store the same compounds though feeding upon taxonomically diverse plant species. A bitter cyanoglycoside, sarmentosin, was characterised from several moth species in the Geometridae, Zygaenidae and Yponomeutidae, and from the apollo butterflies,Parnassius spp. (Papilionidae), although each species feeds on different groups of plants. Interspecific similarities and differences in life history and ecology are discussed in relation to variable characteristics of sequestration of plant compounds among these lepidopteran insects.

Oviposition stimulants for the pipevine swallowtail butterfly,Battus philenor (Papilionidae), from anAristolochia host plant: Synergism between inositols, aristolochic acids and a monogalactosyl diglyceride

Aristolochia macrophylla (Lam.) is a major host of the pipevine swallowtail butterfly,Battus philenor (L.), in the eastern United States. The female butterflies use a synergistic mixture of inositols, acids and a lipid as oviposition cues in recognizing this plant on contact. The acids and lipid, all isolated from the Et2O-CHCl3 fraction of an alcoholic extract of fresh foliage, were identified as aristolochic acid I (1), aristolochic acid II (2) and 1,2-[di(9Z,12Z,15Z)-octadeca-9, 12, 15-trienoyl]-3-galactosyl-sn-glycerol (3). Identifications were facilitated by UV, MS (EI and FAB) and NMR (1D and 2D) spectral techniques and by analysis of the hydrolysis products of 3. The active inositols were identified as D-(+)-pinitol, reported previously, and sequoyitol. Though this is apparently the first report of oviposition responses to a diacyl glycerol glycoside by a phytophagous insect, responses to aristolochic acids and sequoyitol have been reported previously for anAristolochia-feeding swallowtail of a different genus in Japan. This indicates substantial evolutionary conservatism in chemical oviposition cues within the tribe Troidini.

D-(+)-Pinitol, an oviposition stimulant for the pipevine swallowtail butterfly,Battus philenor

Oviposition by females of the pipevine swallowtail butterfly,Battus philenor, was stimulated by contact with alcoholic extracts of host foliage.D-(+)-Pinitol was isolated and identified from leaf material of one host species,Aristolochia macrophylla (Aristolochiaceae). In combination with chloroform-soluble components of host leaf material, this compound was comparable to the parent extract in stimulating oviposition.

Nectar sugar and amino acid preferences of Battus philenor (Lepidoptera, Papilionidae)

Abstract. Butterflies of Battus philenor were tested for their preferences for nectar sugars and amino acids in an outdoor cage experiment. The butterflies clearly preferred both sucrose and fructose over glucose. They also preferred sucrose over fructose. No other preferences were found to be statistically significant, although male butterflies tended to prefer a plain sugar solution over a sugar solution containing a mixture of amino acids: females consumed both of these solutions in almost equal proportions. The results are discussed with respect to nectar composition of butterfly pollinated flowers, flower preferences, physiological and reproductive aspects of butterflies.

Clutch size in the swallowtail butterfly, Battus philenor: the role of host quality and egg load within and among seasonal flights in California

Clutch size in the pipevine swallowtail of California (Battus philenor hirsuta) varies widely within and among two seasonal flights, early and late spring. Pilson and Rausher (1988) proposed that variation in clutch size in a Texan B. philenor population is due to assessment of host quality with subsequent adjustment of clutch size and to differences in motivational state. The assessment hypothesis and a nonexclusive alternative that clutch size is determined by mature egg load were tested for populations in Sacramento, California. Weak and sporadic correlations between host quality and clutch size were found, suggesting that host assessment with adjustment of clutch size is not a strong factor in this population. Clutch size was highly correlated to mature egg load in the early but not in the late spring flight. Yet, females from both flights had similar loads of mature eggs. It is proposed that females lay clutch sizes proportional to egg load, up to a maximum threshold. The threshold may be lowered in the late spring flight in response to changes in overall host quality or to increased egg predation, reducing both the mean clutch size and the correlation between clutch size and egg load. Potential mechanisms for the change in behavior among flights, based on changes in the threshold, are discussed.

The effect of wing orientation on aposematic signalling in the pipevine swallowtail butterfly, Battus philenor

The effect of wing orientation on aposematic signalling in the pipevine swallowtail butterfly, Battus philenor

Sex-limited variability mimicry in the swallowtail butterfly Papilio polyxenes Fabr.

Variation in wing pattern was measured in the swallowtail butterfly Papilio polyxenes, a Batesian mimic of the butterfly Battus philenor. Males and females differed in the number of yellow spots comprising the proximal spot band on the dorsal surfaces of the wings, with females having fewer spots than do males. This difference results in females being more similar to B. philenor than are males. However, females were also more variable in spot number than were males. Full sib analysis of variance of females and regression of daughters on mothers indicates that variation in spot number is heritable. The ventral surfaces of the wings of males and females showed little variability and were similar to those of B. philenor, suggesting that the adaptive significance of the dorsal surface wing pattern differs in males and females. Possible reasons for such a difference are discussed and a model based on the genetics of mimicry in P. polyxenes and developmental studies of wing pattern formation in butterflies is proposed to account for the suppression of variability in male wing pattern.

Egg load influences search intensity, host selectivity, and clutch size inBattus philenor butterflies

Numerous studies have documented the influence of environmental factors such as host plant species and host quality on the oviposition behavior of female insects. This paper shows that an internal physiological factor, the number of mature eggs a female carries (egg load), correlates with host selectivity and clutch size in unmanipulated natural populations of the pipevine swallowtail butterfly, Battus philenor.In addition, search intensity and host selectivity differed among females whose egg loads were manipulated experimentally before they were released and followed in the field. Females with many eggs searched more intensely for hosts and were less selective when they encountered them.