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1. Clonal versus non-clonal milkweeds ( Asclepias spp.) respond differently to stem damage, affecting oviposition by monarch butterflies

   https://doi.org/10.7717/peerj.10296  

   He, Elise ; Agrawal, Anurag A. ( January 2020 , PeerJ)

   Background Oviposition decisions are critical to the fitness of herbivorous insects and are often impacted by the availability and condition of host plants. Monarch butterflies ( Danaus plexippus ) rely on milkweeds ( Asclepias spp.) for egg-laying and as food for larvae. Previous work has shown that monarchs prefer to oviposit on recently regrown plant tissues (after removal of above-ground biomass) while larvae grow poorly on plants previously damaged by insects. We hypothesized that these effects may depend on the life-history strategy of plants, as clonal and non-clonal milkweed species differ in resource allocation and defense strategies. Methodology/Principal Findings We first confirmed butterfly preference for regrown tissue in a field survey of paired mowed and unmowed plots of the common milkweed A. syriaca . We then experimentally studied the effects of plant damage (comparing undamaged controls to plants clipped and regrown, or damaged by insects) on oviposition choice, larval performance, and leaf quality of two closely related clonal and non-clonal species pairs: (1) A. syriaca and A. tuberosa , and (2) A. verticillata and A. incarnata . Clonal and non-clonal species displayed different responses to plant damage, impacting the proportions of eggs laid on plants. Clonal species had similar meanmore »proportions of eggs on regrown and control plants (≈35–40% each), but fewer on insect-damaged plants (≈20%). Meanwhile non-clonal species had similar oviposition on insect-damaged and control plants (20–30% each) but more eggs on regrown plants (40–60%). Trait analyses showed reduced defenses in regrown plants and we found some evidence, although variable, for negative effects of insect damage on subsequent larval performance. Conclusions/Significance Overall, non-clonal species are more susceptible and preferred by monarch butterflies following clipping, while clonal species show tolerance to clipping and induced defense to insect herbivory. These results have implications for monarch conservation strategies that involve milkweed habitat management by mowing. More generally, plant life-history may mediate growth and defense strategies, explaining species-level variation in responses to different types of damage.« less
2. Cardenolides, toxicity, and the costs of sequestration in the coevolutionary interaction between monarchs and milkweeds

   https://doi.org/10.1073/pnas.2024463118  

   Agrawal, Anurag A. ; Böröczky, Katalin ; Haribal, Meena ; Hastings, Amy P. ; White, Ronald A. ; Jiang, Ren-Wang ; Duplais, Christophe ( April 2021 , Proceedings of the National Academy of Sciences)

   For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring–containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch’s neural Na⁺/K⁺-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch’s typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs ofmore »sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.

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3. Video surveillance reveals a community of largely nocturnal Danaus plexippus (L.) egg predators

   https://doi.org/10.1007/s10841-020-00248-w  

   Myers, Andrew T. ; Haan, Nathan L. ; Landis, Douglas A. ( May 2020 , Journal of Insect Conservation)

   Monarch butterfly (Danaus plexippus L.) declines in eastern North America have prompted milkweed host plant restoration efforts in non-agricultural grasslands. However, grasslands harbor predator communities that exert high predation pressure on monarch eggs and larvae. While diurnal monarch predators are relatively well known, no studies have investigated the contribution of nocturnal monarch predators. We used video cameras to monitor sentinel monarch eggs and fourth instars on milkweed in southern Michigan to identify predators and determine if nocturnally-active species impose significant predation pressure. We observed ten arthropod taxa consuming monarch eggs and larvae, with 74% of egg predation events occurring nocturnally. Taxa observed attacking monarch eggs included European earwigs (Forficula auricularia L.), tree crickets (Oecanthus sp.), lacewing larvae (Neuroptera), plant bugs (Miridae), small milkweed bugs (Lygaeus kalmii Stal), ants (Formicidae), spiders (Araneae: Salticidae and other spp.), harvestmen (Opiliones), and velvet mites (Trombidiformes: Trombidiidae). Larvae were attacked by ground beetles (Calleida sp.), jumping spiders (Araneae: Salticidae), and spined soldier bugs (Podisus maculiventris Say). Our findings provide important information about monarch predator-prey interactions that could be used to develop strategies to conserve monarchs through reducing predation on early life stages.
4. Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies

   https://doi.org/10.3390/insects10080253  

   Majewska, Ania A. ; Altizer, Sonia ( August 2019 , Insects)

   Background: North American monarchs (Danaus plexippus) are well-known for their long-distance migrations; however, some monarchs within the migratory range have adopted a resident lifestyle and breed year-round at sites where tropical milkweed (Asclepias curassavica) is planted in the southern coastal United States. An important question is whether exposure to exotic milkweed alters monarch migratory physiology, particularly the ability to enter and remain in the hormonally-induced state of reproductive diapause, whereby adults delay reproductive maturity. Cued by cooler temperatures and shorter photoperiods, diapause is a component of the monarch’s migratory syndrome that includes directional flight behavior, lipid accumulation, and the exceptional longevity of the migratory generation. Methods: Here, we experimentally test how exposure to tropical milkweed during the larval and adult stages influences monarch reproductive status during fall migration. Caterpillars reared under fall-like conditions were fed tropical versus native milkweed diets, and wild adult migrants were placed in outdoor flight cages with tropical milkweed, native milkweed, or no milkweed. Results: We found that monarchs exposed to tropical milkweed as larvae were more likely to be reproductively active (exhibit mating behavior in males and develop mature eggs in females) compared to monarchs exposed to native milkweed. Among wild-caught fall migrants, females exposedmore »to tropical milkweed showed greater egg development than females exposed to native or no milkweed, although a similar response was not observed for males. Conclusions: Our study provides evidence that exposure to tropical milkweed can increase monarch reproductive activity, which could promote continued residency at year-round breeding sites and decrease monarch migratory propensity.« less
5. Impacts of larval host plant species on dispersal traits and free-flight energetics of adult butterflies

   https://doi.org/10.1038/s42003-022-03396-8  

   Pocius, Victoria M. ; Cibotti, Staci ; Ray, Swayamjit ; Ankoma-Darko, Obenewa ; McCartney, Nathaniel B. ; Schilder, Rudolf J. ; Ali, Jared G. ( May 2022 , Communications Biology)

   Animals derive resources from their diet and allocate them to organismal functions such as growth, maintenance, reproduction, and dispersal. How variation in diet quality can affect resource allocation to life-history traits, in particular those important to locomotion and dispersal, is poorly understood. We hypothesize that, particularly for specialist herbivore insects that are in co-evolutionary arms races with host plants, changes in host plant will impact performance. From their coevolutionary arms-race with plants, to a complex migratory life history, Monarch butterflies are among the most iconic insect species worldwide. Population declines initiated international conservation efforts involving the replanting of a variety of milkweed species. However, this practice was implemented with little regard for how diverse defensive chemistry of milkweeds experienced by monarch larvae may affect adult fitness traits. We report that adult flight muscle investment, flight energetics, and maintenance costs depend on the host plant species of larvae, and correlate with concentration of milkweed-derived cardenolides sequestered by adults. Our findings indicate host plant species can impact monarchs by affecting fuel requirements for flight.