An energetic analysis of host plant selection by the large milkweed bug,Oncopeltus fasciatus

Summary The large milkweed bug, Oncopeltus fasciatus, is a specialized seed feeder that has been observed completing nymphal development in the field on only a small proportion of its potential host species within the genus Asclepias. In central Missouri only two of the six milkweed species studied, A. syriaca and A. verticillata, commonly supported nymphal O. fasciatus growth in the field. The seed of all six species, however, was equally suitable food for bugs reared in the laboratory. In laboratory preference tests, adult bugs chose to feed on the largest seeds, A. hirtella, but such a preference could not explain the observed field feeding patterns.One explanation to account for the observed host plant selection is based upon an energetic analysis. Only A. syriaca provided enough seed biomass for a clutch of O. fasciatus nymphs to develop on a single plant, and only A. verticillata grew in high enough density that a clutch could find sufficient food within the limited range of nymphal movement. These results illustrate a corollary of the resource concentration hypothesis: within a plant group whose members share similar secondary plant chemistries, the only species that will be viable hosts for a specialized herbivore are those that provide the minimal resource density necessary for the completion of nymphal development.In central Missouri, O. fasciatus has specialized on a critical resource density, not traits of individual Asclepias species. The appearance of host selection within the potential host plant spectrum is the result of a characteristic growth form, seed output, and dispersion pattern for each milkweed species that makes some species much more likely than others to produce sufficient seed resources.     

Nerium oleander as an alternative host plant for south Florida milkweed bugs, Oncopeltus fasciatus

Abstract.

• 1 Life history data were gathered for south Florida Oncopeltus fasciatus reared from eggs on Nerium oleander seeds and milkweed seeds in the laboratory.
• 2 Milkweed seeds were found to be a superior food source since O.fasciatus grew faster, laid more clutches, and has a higher total fecundity on milkweed seeds.
• 3 Fruiting N.oleander was found to be a better food source than nonfruiting milkweeds in a summer field study in south Florida since no nymphs survived to the adult stage on nonfruiting milkweeds but some did on N.oleander.
• 4 O.fasciatus adults and nymphs are abundant on N.oleander in the summer in south Florida when N.oleander is fruiting; no O.fasciatus nymphs are found in the summer on the milkweeds which are not fruiting.
• 5 O.fasciatus leave N.oleander in the autumn when milkweeds start to fruit and can then be found on fruiting milkweeds.

     

The effect of host plant phenology on reproduction of the milkweed bug,Oncopeltus fasciatus,in tropical Florida

Summary A field study of the relationship between host plant phenology and the reproductive pattern of the large milkweed bug, Oncopeltus fasciatus, was conducted in south Florida. Since O. fasciatus need seeds of either milkweed or Nerium oleander plants to reproduce, reproduction takes place on only those host plants that are producing seed pods.Two of four major host plants, Asclepias incarnata and Sarcostemma clausa fruit seasonally, producing pods in early autumn and early winter, respectively. The third milkweed host, Asclepias curassavica, produces almost no pods midsummer (although it flowers abundantly) and few pods midwinter. Nerium oleander (Apocynaceae) produces some pods all year but is only used by O. fasciatus in the summer when milkweeds are not producing pods. Correspondingly, reproduction of O. fasciatus has been observed year round, but relatively few females reproduce in midwinter, coinciding with decreased pod production and low temperatures. This pattern is consistent with the hypothesis that a photoperiodic cue of short day lengths under conditions of cool temperatures may cause adult females to enter diapause and delay reproduction in the field.A comparison of plant phenologies and rainfall between 1976, a very dry year, and 1978, a year with normal rainfall, showed that extreme dryness disrupted the seasonal fruiting of the milkweeds and consequently the reproduction of O. fasciatus.     

Olfactory responses to milkweed seed extracts in the milkweed bug

Electrophysiological studies showed that milkweed seed extracts have compounds which are stimulating to the olfactory chemoreceptors of the adult milkweed bug, Oncopeltus fasciatus. Ethanol extracts were the most stimulatory. These compounds may function as feeding attractants or stimulants. Sex, starvation, and mating did not affect the olfactory chemoreceptor responses.     

Chemical egg defence in the large milkweed bug,Oncopeltus fasciatus,derives from maternal but not paternal diet

Many herbivorous insects sequester defensive compounds from their host‐plants and incorporate them into their eggs to protect them against predation. Here, we investigate whether transmission of cardenolides from the host‐diet to the eggs is maternal, paternal, or biparental in the large milkweed bug, Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). We reared individual bugs on either milkweed seeds [MW; Asclepias syriaca L. (Apocynaceae)] that contain cardenolides, or on sunflower seeds [SF; Helianthus annuus L. (Asteraceae)] that do not contain cardenolides. We mated females and males so that all four maternal/paternal diet combinations were represented: MW/MW, MW/SF, SF/MW, and SF/SF. Using larvae of the common green lacewing, Chrysoperla (Chrysopa) carnea (Stevens) (Neuroptera: Chrysopidae), we conducted two‐choice predation trials to assess whether maternal, paternal, or biparental transmission of cardenolides into the eggs of O. fasciatus increased protection against predation. Furthermore, we used high performance liquid chromatography (HPLC) to assess putative cardenolide content of eggs from the various parental diet treatment groups. The predation trials suggested that regardless of male diet, eggs were afforded better protection when females had been raised on milkweed. However, many eggs were at least partially consumed. This suggests that although chemical defence of eggs does not guarantee protection to eggs on an individual basis, they may increase the probability that some eggs in a clutch are left intact thereby potentially conferring a fitness advantage to more offspring than if eggs are left unprotected. Based on HPLC analysis we found that maternal contribution of cardenolides was significantly greater than paternal contribution of cardenolides to the eggs, supporting the results of our predation trials that a maternal diet of milkweed makes eggs more distasteful than a paternal diet of milkweed.     

Cardenolide‐defended milkweed bugs do not evoke learning in Nephila senegalensis spiders

Antipredator defense of herbivorous insects often relies on the potential toxicity of defensive chemicals sequestered from their host plants. The colorful Lygaeinae (Heteroptera: Lygaeidae) store a concentrated mixture of toxic cardenolides (cardiac glycosides) in specialized storage compartments of the bugs' integument, from which they are released upon attack. Larvae and adults of the large milkweed bug Oncopeltus fasciatus (Heteroptera: Lygaeinae) are specialized to feed on cardenolide‐containing milkweeds in the plant genus Asclepias and display a conspicuous red and black colorations. To investigate whether O. fasciatus gained improved protection by feeding on a toxic host plant (Asclepias syriaca), compared to a nontoxic alternative (sunflower seeds), we fed nymphs and adults of O. fasciatus to the golden orb‐weaver Nephila senegalensis. While visually oriented vertebrates, such as avian predators, have been intensively investigated for their reaction to defensive compounds and aposematic coloration, less attention has been paid to invertebrate predators. Their different perceptual abilities can provide important opportunities for testing hypotheses on warning coloration and chemical defenses. The predation trials showed that the bugs fed on Asclepias were significantly less likely to be killed than the bugs reared on a cardenolide‐free diet. This suggests that sequestered cardenolides in O. fasciatus nymphs and adults represent a significant fitness advantage on an individual level against this invertebrate predator. Yet, when testing for avoidance learning in the spiders, negative experience did not change the way how similar prey was attacked at the next encounter. In this case, visual or chemical aposematism thus does not seem to matter for predator learning.     

DIRECT AND CORRELATED RESPONSES TO SELECTION AMONG LIFE-HISTORY TRAITS IN MILKWEED BUGS (ONCOPELTUS FASCIATUS)

Offspring-parent regressions provided initial estimates of heritabilities and genetic correlations among wing length, body length, pronotum width, head-capsule width, development time, age at first reproduction, and fecundity in an Iowa population of the large milkweed bug, Oncopeltus fasciatus. Replicated, bidirectional selection for wing length was imposed for nine generations. The direct response to selection revealed the existence of substantial additive genetic variance for wing length in this population. Traits were assayed for correlated responses to selection after seven generations. Body length, pronotum width, head capsule width, and fecundity showed consistent, positive correlated responses. Development time showed a negative correlated response. Age at first reproduction showed no consistent correlated response to selection on wing length. These pleiotropic effects among wing length and fecundity, development time, and body size characters provide the potential for these traits to evolve together in O. fasciatus, independently of age at first reproduction.     

Identification of the adipokinetic hormone of the large milkweed bug Oncopeltus fasciatus

Abstract The adipokinetic hormone (AKH) of the large milkweed bug Oncopeltus fasciatus is isolated from an acidified methanolic extract of 200 corpora cardiaca, purified by single step reversed phase high‐performance liquid chromatography (HPLC) and N‐terminally deblocked using pyroglutamate aminopeptidase. The sequence is identified by Edman degradation and matrix assisted laser desorption/ionization‐time of flight mass spectroscopy as pGlu‐Leu‐Asn‐Phe‐Ser‐Pro‐Asn‐Trp amide. This structure is confirmed by chemical synthesis and coelution of native and synthetic peptide on HPLC. The AKH of O. fasciatus is identical to Tenmo‐HrTH, a member of the adipokinetic/red pigment‐concentrating hormone peptide family that had been isolated earlier from several tenebrionid beetles. Tenmo‐HrTH causes a significant rise in the concentration of haemolymph lipids when injected into adult male and female O. fasciatus, but displays no hyperglycaemic activity. There is no indication of the presence of other AKHs in O. fasciatus. The large milkweed bug represents the first member of the seed bugs (Lygaeidae) for which the endogenous AKH has been identified.     

Jumping spiders attend to context during learned avoidance of aposematic prey

A large number of studies on both animals and humans have demonstratedthat learning is influenced by context or secondary cues thatare present when an association is formed. Few studies, however,have examined the functional value of attending to context.We first demonstrated that jumping spiders, Phidippus princeps,could be trained to avoid aposematic, distasteful milkweed bugs,Oncopeltus fasciatus. Spiders readily attacked bugs on firstexposure but were significantly less likely to do so after eighttrials, although they subsequently attacked and ate crickets.Spiders exposed to nontoxic milkweed bugs reared on sunflowerseeds did not show the same decline in attack rate. We nextexamined the effects of secondary contextual cues on spiderlearning by training spiders to avoid milkweed bugs in one oftwo environments. When spiders were tested in an environmentdifferent from the one in which they were trained, attack ratesincreased, and spiders no longer demonstrated retention of theassociation. Spiders tested in the same environment in whichthey were trained continued to avoid attacking the bugs. Theseresults have potential consequences for the evolution of bothpredator and prey and point to the importance of studying context-dependentlearning.     

Dietary influence of cardenolides on larval growth and development of the milkweed bug Oncopeltus fasciatus

Larvae of the milkweed bug Oncopeltus fasciatus were reared on the seeds of eight different species of milkweed (Asclepias), representing a wide range of cardenolide concentrations in the diet. There were few significant differences in larval developmental period, wet body weight of teneral adults, dry weight of adults, and pronotal width of adults reared on the different diets. However, the data indicate no significant correlations between cardenolide content, and body weight or size of the adult insects.There was no evidence in this study of a physiological cost or adverse effect on the larval growth and development of insects which sequestered and stored differing quantities of cardenolides. Instead, the data support a recently-proposed model of cardenolide sequestration which may be energy-independent.The validity of evidence supporting a physiological cost hypothesis for sequestration of cardenolides by the monarch butterfly is discussed in the light of these findings.     

ZUR FRAGE DER WIRTSSPEZIFITÄT BEI ONCOPELTUS FASCIATUS (HETEROPTERA: LYGAEIDAE)

Zusammenfassung Die Frage der Wirtsspezifität von Oncopeltus fasciatus Dall. wurde unter Verwendung der Samen von Asclepias syriaca, Helianthus annuus und Arachis hypogaea untersucht. Die eindeutige Bevorzugung von A. syriaca gegenüber den Samen von Helianthus und Arachis beruht auf einer oder mehreren Substanzen in der Samenschale von Asclepias, die den Anstich auslösen. Diese Substanz(en) läßt (lassen) sich extrahieren und auf Helianthus-Samen übertragen. Milchröhreninhalt von A. syriaca-Pflanzen zeigt denselben Effekt. Die Lygaeide Oncopeltus fasciatus kann jedoch mit H. annuus-Samen ernährt und erfolgreich gezüchtet werden. Entwicklungsgeschwindigkeit und Reproduktion sind zwar vermindert, Lebensdauer und Eigewichte aber auf beiden Wirten identisch. Zuchtversuche mit Samen von Arachis hypogaea dagegen verliefen erfolglos.

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Summary The host specificity of the lygaeid Oncopeltus fasciatus feeding on seeds of Asclepias syriaca, Helianthus annuus and Arachis hypogaea has been investigated. The bug clearly prefers seeds of A. syriaca over seeds of A. hypogaea and H. annuus though the latter are also accepted. Stylet penetration is stimulated by unidentified chemical factors occurring in the milkweed seed coat. It is assumed that this stimulation increases the frequency of feeding acts and thus the volume of uptaken food. An extract of the seed shell of A. syriaca was coated on the surface of Helianthus seeds. After this treatment the bug was stimulated to penetrate the latter. The same effect was obtained with the milky latex of Asclepias plants. O. fasciatus can be reared on seeds of H. annuus successfully. The speed of development and the reproduction capacity are diminished but the longevity and the weight of the eggs on both hosts (A. syriaca and H. annuus) are identical. Seeds of A. hypogaea, on the contrary, appeared to be totally unsuitable as a rearing substrate.

     

Plant abandonment behavior and fitness of monarch larvae (Danaus plexippus) is not influenced by an intraspecific competitor

Integrating aspects of larval lepidopteran behavior that enhance survival into conservation plans could increase the overall impact of the efforts. We previously recommended that where possible, maintaining 2–4 ramets of closely-spaced common milkweed would support the development of at least one monarch through pupation, based on a seemingly innate behavior in which monarch larvae (Danaus plexippus) abandon their natal milkweed ramet (Asclepias sp.). Here, we explored the impact of intraspecific competition on larval ramet abandonment behavior and fitness of monarch larvae in small artificial milkweed patches.

We observed larvae reared under direct and indirect intraspecific competition, and larvae reared alone.

We found no influence of intraspecific competition; however, our study provides further support that milkweed ramet abandonment is a seemingly innate behavior. This behavior occurs before all of the available leaf biomass on a ramet is consumed and prior to the pre-pupal wandering stage.

Implications for insect conservation: Results from our study suggest that in the absence of predation, parasitism, and interspecific competition, and when sufficient plant biomass is present to support larval development, the presence of an intraspecific competitor does not influence larval behavior or fitness. Based on milkweed ramet abandonment behavior, we continue to suggest maintaining small patches of 2–4 milkweed ramets when possible.

     

Responses of the large milkweed bug, Oncopeltus fasciatus (Hemiptera: Lygaeidae) to chemically defined diets

The large milkweed bug, Oncopeltus fasciatus (Dallas), was reared from fourth instar to the adult stage on chemically defined diets, and was maintained alive for 2 to 5 months on such diets. Insects grew better on diets containing 5% sucrose than on those containing 3, 10 or 20% sucrose, and gained almost as much weight as those on milkweed seed and water. Newly hatched nymphs gained almost ten times in weight and moulted once or twice on different diet solutions, but never reached the adult stage. Diluted diets greatly prolonged the length of the stadium and survival of first- and second-instar nymphs, but these did not reach the adult stage. Ommission of cholesterol from the diet had no effect either on growth or moulting of this insect.

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Résumé On a pu élever la punaise de l'asclépiade, Oncopeltus fasciatus (Dallas) sur des régimes de composition chimique définie, ceci à partir du quatrième stade larvaire jusqu'à l'imago, et la maintenir sur de tels régimes durant deux à cinq mois consécutifs. La croissance pondérale de l'insecte a été supérieure sur les régimes contenant 5% de sucrose que sur ceux contenant 3, 10 ou 20% de sucrose, et est comparblle à celle obtenue sur les régimes à base de graines d'asclépiade. La croissance des larves fra?chement écloses placées sur de tels régimes a été décuplée; ces larves ont mué une ou deux fois, sans toutefois atteindre le stade adulte. Des régimes dilués ont eu pour effet de prolonger considérablement la survie et la durée des larves de premier et deuxième stades. Labsence de cholestérol dans les régimes nutritifs a semblé n'avoir aucun effet sur la croissance et la mue.

     

Natural food requirements of the large milkweed bug,Oncopeltus fasciatus (Hemiptera: Lygaeidae), and their relation to gregariousness and host plant morphology

Summary The life ofOncopeltus fasciatus centers on the seeds of milkweeds (Asclepiadaceae,Asclepias syriaca in this study). Adults reproduce prolifically on these seeds, but they engage in only half as much copulation and lay only a few eggs when fed milkweed buds and flowers instead. They can not maintain body weight on a diet of just vegetative plants. Vegetative shoots support only slow growth and produce adults only in certain circumstances.Seeds are often inaccessible to nymphs in the three youngest instars, since their mouthparts are too short to penetrate the thick walls ofA. syriaca pods. Nymphs feeding from the outside of closed pods develop more slowly than those feeding on exposed seeds. Since mortality occurs at a constant rate, slow growth results in fewer surviving. Even adults, which can feed through almost any pod wall, prefer to feed where it is thinnest. Thus the pod wall effectively protects many seeds from this herbivore.Nymphs in larger groups (20 individuals) suffer much lower mortality than those in small groups (5 individuals), when they are feeding from the outside of closed pods. However, group size does not affect survival when nymphs are fed seed. Gregariousness apparently partly compensates for the less nutritious diet attainable from the outside of pods and thus is related to this bug's extreme specialization of diet.Other characteristics coordinated with the seed requirement include the timing of migration and egg laying, the female's choice of oviposition site, and the nymphs' balanced tendencies to be sedentary and to disperse. Among the milkweeds, such traits as thick pod walls, wide spacing, and rapid seed dispersal could have been selected for by a seed predator such asO. fasciatus.As a specialist and a probable agent of such selection,O. fasciatus is committed to keeping up with changes in its host plant. This requires maintaining some flexibility in its behavior or gene pool. K. Evans (personal communication) finds thatO. fasciatus in California onA. fascicularis lays eggs so early that the first nymphs hatch as the first flowers are opening. In that more equitable climate and on that host, adult reproduction is apparently not as dependent on pods being present in the colonized patch, and the nymphs must rely on non-seed food more often than they do in the association withA. syriaca in the East and Midwest. This very specialized species apparently retains enough adaptability to exploit milkweeds of various forms and phenologies living in a wide range of climates. This adaptability could promise its continued success in the coevolutionary race with its host plants.     

Juvadecene: Discovery of a juvenile hormone mimic in the plant,Macropiper excelsum

A compound with significant insect juvenile hormone activity was isolated from the plant, Macropiper excelsum. The chemical structure was determined by spectral methods to be 1-(3,4-methylenedioxyphenyl)-trans-3-decene(l), and confirmed by synthesis. The hormonally active substance applied topically to last (fifth)-instar nymphs of the milkweed bug (Oncopeltus fasciatus) induced a supernumerary metamorphosis at 30 μg. Higher doses were toxic.     

Comparative pattern of genetic structure in two Mediterranean killifishes Aphanius fasciatus and Aphanius iberus inferred from both mitochondrial and nuclear data

In this study, genetic variation was assessed in Aphanius fasciatus and Aphanius iberus characterized by similar ecological traits but with very different distribution ranges in the Mediterranean area. Five populations of A. iberus and five of A. fasciatus were analysed using five polymorphic microsatellite loci and partial mitochondrial control region (D‐loop) sequences. Congruent results were found with both nuclear and mitochondrial molecular markers. The results showed that similar levels of genetic divergence, based on mitochondrial control region sequences, are present among populations of A. iberus and among populations of A. fasciatus despite the very different geographic distance existing among the examined populations of the two species (low geographic distance in A. iberus and high in A. fasciatus). A possible explanation could be that the populations of A. iberus were isolated for a longer time than the populations of A. fasciatus supporting the hypothesis that the split in the lineage leading to A. iberus is older than the split in the lineage leading to A. fasciatus. The possibility that the wide circum‐Mediterranean distribution of A. fasciatus ensures the high connectivity of its populations, preventing, in some cases, local differentiation, however, cannot be ruled out.     

The role of maternal effects in adaptation to different diets

The environmental influences of mothers on offspring traits, or maternal effects, often arise from dietary differences experienced by mothers. However, few studies have explored if and how maternal effects facilitate adaptation to new host plants. To address this, we compared the maternal and direct effects arising from dietary differences in two populations of the large milkweed bug, Oncopeltus fasciatus that live on and feed on the seeds from different hosts. We compared a laboratory population, which has been reared for over 400 generations on sunflower seeds and is now adapted to use these as a host, to the wild population, which is adapted to the ancestral diet of toxic milkweed seeds. We first tested for changes in maternal effects, and then examined offspring performance and survivorship. We found evidence for evolution of the maternal effect facilitating the use of a novel host. However, the strongest effects were population differences and direct dietary effects for all traits. Offspring performance was more strongly influenced by diet than maternal effects. Survivorship depended on population and offspring diet, and their interaction, but was unaffected by maternal diet or other interactions. In the artificially evolved population, diet breadth was increased rather than evolving specialization. Our results suggest changes in maternal effects are likely to be weak compared to direct effects of host plants and other adaptations in adaptation to a novel host. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 202–211.     

Insect Feeding Deterrents in Endophyte-Infected Tall Fescue

The presence of an endophytic fungus, Acremonium coenophialum, in tall fescue (Festuca arundinacea) deterred aphid feeding by Rhopalosiphum padi and Schizaphis graminum. Both species of aphid were unable to survive when confined to endophyte-infected tall fescue plants. Feeding deterrents and toxic factors to R. padi and Oncopeltus fasciatus, large milkweed bug, were primarily associated with a methanol extract obtained when endophyte-infected tall fescue seed was serially extracted with hexane, ethyl acetate, and methanol. The concentrations of pyrrolizidine alkaloids were determined to be 30 to 100 times greater in the methanol extract than in the hexane and ethyl acetate extracts.     

Stable isotopes (δD and δ13C) are geographic indicators of natal origins of monarch butterflies in eastern North America

Wing membranes of laboratory and field-reared monarch butterflies (Danaus plexippus) were analyzed for their stable-hydrogen (δD) and carbon (δ¹³C) isotope ratios to determine whether this technique could be used to identify their natal origins. We hypothesized that the hydrogen isotopic composition of monarch butterfly wing keratin would reflect the hydrogen isotope patterns of rainfall in areas of natal origin where wings were formed. Monarchs were reared in the laboratory on milkweed plants (Asclepias sp.) grown with water of known deuterium content, and, with the assistance of volunteers, on native milkweeds throughout eastern North America. The results show that the stable hydrogen isotopic composition of monarch butterflies is highly correlated with the isotopic composition of the milkweed host plants, which in turn corresponds closely with the long-term geographic patterns of deuterium in rainfall. Stable-carbon isotope values in milkweed host plants were similarly correlated with those values in monarch butterflies and showed a general pattern of enrichment along a southwest to northeast gradient bisecting the Great Lakes. These findings indicate that natal origins of migratory and wintering monarchs in Mexico can be inferred from the combined δD and δ¹³C isotopic signatures in their wings. This relationship establishes that analysis of hydrogen and carbon isotopes can be used to answer questions concerning the biology of migratory monarch butterflies and provides a new approach to tracking similar migratory movements of other organisms. Received: 1 July 1998 / Accepted: 11 November 1998