Effect of food limitation on food consumption and reproductive allocation by adult milkweed bugs, Oncopeltus fasciatus

Male/female pairs of adult milkweed bugs, Oncopeltus faciatus were offered reduced food rations (100 mg milkweed seeds/week, 50 mg seeds/week, and 25 mg seeds/week) at 232C, 14L : 10D photoperiod. The high rate of food consumption normally occurring during the teneral period (first 8 days posteclosion) and subsequent food consumption were reduced on both reduced rations. Initial fresh weight was lost by bugs on both reduced rations and their weekly fresh body weight tended to remain less than bugs on the 100 mg seeds/week ration.Normal onset of egg production (about 3 weeks posteclosion) was delayed 6 weeks and normal length of a female's life (13–14 weeks) was increased 7–8 weeks on the 25 mg seeds/week ration. Rate of egg production exhibited a linear decrease with decrease in food ration on both reduced rations due to an increased interclutch interval, while fresh egg weight, duration of egg stage, number of eggs/clutch and percentage of clutches containing fertile eggs were little affected.Gross egg production efficiency (efficiency of conversion of ingested food into eggs = dry mg egg production × 100/dry mg food ingested) was high on both the 100 and 50 mg seeds/week rations (27.9% and 21.1%, respectively) and low (7.7%) on the 25 mg seeds/week ration. These data are discussed in the context of the reciprocal interaction between nutrient intake and egg production.     

Sex-determined differential mortality of milkweed bugs, Oncopeltus fasciatus (hemiptera), to aflatoxins

Studies on the aflatoxins, toxic metabolites of Aspergillus flavus and A. parasiticus, have involved test systems ranging from cell cultures to laboratory animals. This work reports on the differential response by sex of Oncopeltus fasciatus to aflatoxin B₁ (AFB₁). Young adult milkweed bugs were chosen randomly from our stock colony and housed in glass culture jars. Triplicate sets of experimental animals were fed 5 μg/ml of AFB₁ in their liquid diet. The first death for the experimental females occurred at day 4, and at 10 days for the experimental males. A 50% lethality level for experimental females developed by day 8. Males subjected to the same concentration achieved a 50% lethality level at day 24. For the females the LD₅₀ occurred after consuming 0.49 μg/ml of AFB₁. The results indicate that adult female milkweed bugs were hypersensitive to AFB₁ as compared to adult males. This organism is more sensitive than the American cockroach and less sensitive than the fruitfly, housefly, and honeybee to toxic aflatoxicosis. Even the female is not sufficiently sensitive to rate highly as a bioassay organism for AFB₁. The extreme difference in mortality between the sexes is significant, unusual, and unexplained.     

Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies

Host resistance to parasites can come in two main forms: hosts may either reduce the probability of parasite infection (anti-infection resistance) or reduce parasite growth after infection has occurred (anti-growth resistance). Both resistance mechanisms are often imperfect, meaning that they do not fully prevent or clear infections. Theoretical work has suggested that imperfect anti-growth resistance can select for higher parasite virulence by favouring faster-growing and more virulent parasites that overcome this resistance. In contrast, imperfect anti-infection resistance is thought not to select for increased parasite virulence, because it is assumed that it reduces the number of hosts that become infected, but not the fitness of parasites in successfully infected hosts. Here, we develop a theoretical model to show that anti-infection resistance can in fact select for higher virulence when such resistance reduces the effective parasite dose that enters a host. Our model is based on a monarch butterfly-parasite system in which larval food plants confer resistance to the monarch host. We carried out an experiment and showed that this environmental resistance is most likely a form of anti-infection resistance, through which toxic food plants reduce the effective dose of parasites that initiates an infection. We used these results to build a mathematical model to investigate the evolutionary consequences of food plant-induced resistance. Our model shows that when the effective infectious dose is reduced, parasites can compensate by evolving a higher per-parasite growth rate, and consequently a higher intrinsic virulence. Our results are relevant to many insect host-parasite systems, in which larval food plants often confer imperfect anti-infection resistance. Our results also suggest that - for parasites where the infectious dose affects the within-host dynamics - vaccines that reduce the effective infectious dose can select for increased parasite virulence.     

Plant water stress and previous herbivore damage affect insect performance

1. Short‐term changes in plant resistance traits can be affected by abiotic factors or damage by herbivores, although how the combined effects of abiotic factors and previous damage affect subsequent insect larval development is not well understood. 2. Complementary glasshouse and field experiments were conducted to evaluate whether plant water stress and previous herbivore damage influenced monarch (Danaus plexippus) larval development on common milkweed, Asclepias syriaca. 3. In the glasshouse, water stress altered a suite of A. syriaca functional traits but did not affect nutrient content, whereas herbivore damage increased leaf nitrogen (N) and reduced the carbon:nitrogen (C:N) ratio. A bioassay experiment showed that monarch larval survival was lower on well‐watered plants that were previously damaged by monarch larva than on damaged and drought‐stressed plants. Bioassay larvae consumed less leaf tissue of previously damaged plants, whereas monarch larval mass was affected additively by water stress and previous damage, after correcting for the amount of leaf tissue consumed. 4. In a 2‐year field experiment, monarch larval performance was higher on previously damaged A. syriaca plants that received experimentally reduced rainfall, relative to plants receiving ambient rainfall. 5. Collectively, these results from glasshouse and field experiments suggest that insect performance was highest on previously damaged plants under water stress and highlight the additive and interactive roles of abiotic and biotic factors on herbivore performance.     

FOOD PLANT DERIVED DISEASE TOLERANCE AND RESISTANCE IN A NATURAL BUTTERFLY‐PLANT‐PARASITE INTERACTIONS

Organisms can protect themselves against parasite‐induced fitness costs through resistance or tolerance. Resistance includes mechanisms that prevent infection or limit parasite growth while tolerance alleviates the fitness costs from parasitism without limiting infection. Although tolerance and resistance affect host–parasite coevolution in fundamentally different ways, tolerance has often been ignored in animal–parasite systems. Where it has been studied, tolerance has been assumed to be a genetic mechanism, unaffected by the host environment. Here we studied the effects of host ecology on tolerance and resistance to infection by rearing monarch butterflies on 12 different species of milkweed food plants and infecting them with a naturally occurring protozoan parasite. Our results show that monarch butterflies experience different levels of tolerance to parasitism depending on the species of milkweed that they feed on, with some species providing over twofold greater tolerance than other milkweed species. Resistance was also affected by milkweed species, but there was no relationship between milkweed‐conferred resistance and tolerance. Chemical analysis suggests that infected monarchs obtain highest fitness when reared on milkweeds with an intermediate concentration, diversity, and polarity of toxic secondary plant chemicals known as cardenolides. Our results demonstrate that environmental factors—such as interacting species in ecological food webs—are important drivers of disease tolerance.     

Maintenance of narrow diet breadth in the monarch butterfly caterpillar: response to various plant species and chemicals

In order to better understand the maintenance of a fairly narrow diet breadth in monarch butterfly larvae, Danaus plexippus L. (Lepidoptera: Nymphalidae: Danainae), we measured feeding preference and survival on host and non-host plant species, and sensitivity to host and non-host plant chemicals. For the plant species tested, a hierarchy of feeding preferences was observed; only plants from the Asclepiadaceae were more or equally preferred to Asclepias curassavica, the common control. The feeding preferences among plant species within the Asclepiadaceae are similar to published mean cardenolide concentrations. However, since cardenolide data were not collected from individual plants tested, definitive conclusions regarding cardenolide concentrations and plant acceptability cannot be made. Although several non-Asclepiadaceae were eaten in small quantities, all were less preferred to A. curassavica. Additionally, these non-Asclepiadaceae do not support continued feeding, development, and survival of first and fifth-instar larvae. Preference for a host versus a non-host (A. curassavica versus Vinca rosea) increased for A. curassavica reared larvae as compared to diet-reared larvae suggesting plasticity in larval food preferences. Furthermore, host species were significantly preferred over non-host plant species in bioassays using a host plant or sucrose as a common control. Larval responses to pure chemicals were examined in order to determine if host and non-host chemicals stimulate or deter feeding in monarch larvae. We found that larvae were stimulated to feed by some ubiquitous plant chemicals, such as sucrose, inositol, and rutin. In contrast, several non-host plant chemicals deterred feeding: caffeine, apocynin, gossypol, tomatine, atropine, quercitrin, and sinigrin. Additionally the cardenolides digitoxin and ouabain, which are not in milkweed plants, were neutral in their influence on feeding. Another non-milkweed cardenolide, cymarin, significantly deterred feeding. Extracts of A. curassavica leaves were tested in bioassays to determine which components of the leaf stimulate feeding. Both an ethanol extract of whole leaves and a hexane leaf-surface extract are phagostimulatory, suggesting the involvement of both polar and non-polar plant compounds. These data suggest that the host range of D. plexippus larvae is maintained by both feeding stimulatory and deterrent chemicals in host and non-host plants.     

Contact chemoreception related to host selection and oviposition behaviour in the monarch butterfly, Danaus plexippus

Abstract. Behavioural events during host selection by ovipositing monarch butterflies (Danaus plexippus (L.), Danainae, Nymphalidae) include tapping the leaf surface with fore-tarsi and touching this surface with mid-tarsi (‘drumming’) and antennae. Flavonoids identified from host plant extracts are known to stimulate oviposition. Scanning electron microscopy revealed the presence of contact-chemoreceptor sensilla on all appendages that contact the leaf surface. This electrophysiological study was conducted to identify the contact chemoreceptors that are sensitive to the known oviposition stimuli and are therefore probably involved in host recognition. Receptor cells of conspicuous sensilla grouped in clusters on fore-tarsi of females were sensitive to the behaviourally active butanol fraction of host plant (Asclepias curassavica) extract. However, these receptors generally had low sensitivity to three oviposition-stimulating flavonoids identified from this fraction, but they were also sensitive to the butanol fraction of a non-host (Brassica oleracea). Chemoreceptors in sensilla of the tarsomers 2–4 of the mid-legs also responded to the behaviourally active fraction of host plant extract and showed some sensitivity to two of the flavonoids that stimulate oviposition. Similar results were obtained from receptor cells in sensilla on the tip of the antennae. Most of these sensilla had cells responding to the butanol fraction of A. curassavica extract but only 25% of them were also sensitive to one of the behaviourally active flavonoids. These electrophysiological results, in combination with behavioural observations, suggest that host selection in monarch butterflies relies on a complex pattern of peripheral sensory information from several types of tarsal and antennal contact chemoreceptors.     

Phylogenetic relationships among genera of danaine butterflies (Lepidoptera: Nymphalidae) as implied by morphology and DNA sequences

Cladistic relationships among genera and subtribes of Danaini (the milkweed butterflies) were inferred by analysis of data combined from five sources: morphology of adults and immature stages, and DNA sequences from three gene regions. The results corroborate and greatly increase support for prior hypotheses based on morphology alone. A new index summarizing incongruence among data partitions, the Partition Congruence Proportion (PCP), is introduced. The significance of the inferred pattern of phylogenetic relationships for comparative chemical ecology of milkweed butterflies is briefly discussed.     

Population differences in self-fertility in the “self-incompatible” milkweed Asclepias exaltata (Asclepiadaceae)

Individual plants of Asclepias exaltata (Asclepiadaceae) typically express an unusual self-incompatibility system under single-gene control. Hand-pollinations performed in six natural populations detected occasional self-fertile plants. The frequency of self-fertile individuals ranged from 0 to 34.0% and differed significantly among populations. Self-fertility appears to be under genetic control, as the ability of most plants (80.0 %) to set fruit following self-pollinations was identical under natural and greenhouse conditions. Seed- and fruit-set, however, were significantly lower from self- vs. cross-pollinations. Allozyme analysis of the population with the highest frequency of self-fertility revealed that adult plants were not significantly inbred. Finally, fruit-set following within-population cross-pollinations did not differ from that following wide, between-population cross-pollinations.