skip to main content


Title: Host Plant Species Mediates Impact of Neonicotinoid Exposure to Monarch Butterflies
Neonicotinoids are the most widely used insecticides in North America. Numerous studies document the negative effects of neonicotinoids on bees, and it remains crucial to demonstrate if neonicotinoids affect other non-target insects, such as butterflies. Here we examine how two neonicotinoids (imidacloprid and clothianidin) affect the development, survival, and flight of monarch butterflies, and how these chemicals interact with the monarch’s milkweed host plant. We first fed caterpillars field-relevant low doses (0.075 and 0.225 ng/g) of neonicotinoids applied to milkweed leaves (Asclepias incarnata), and found no significant reductions in larval development rate, pre-adult survival, or adult flight performance. We next fed larvae higher neonicotinoid doses (4–70 ng/g) and reared them on milkweed species known to produce low, moderate, or high levels of secondary toxins (cardenolides). Monarchs exposed to the highest dose of clothianidin (51–70 ng/g) experienced pupal deformity, low survival to eclosion, smaller body size, and weaker adult grip strength. This effect was most evident for monarchs reared on the lowest cardenolide milkweed (A. incarnata), whereas monarchs reared on the high-cardenolide A. curassavica showed no significant reductions in any variable measured. Our results indicate that monarchs are tolerant to low doses of neonicotinoid, and that negative impacts of neonicotinoids depend on host plant type. Plant toxins may confer protective effects or leaf physical properties may affect chemical retention. Although neonicotinoid residues are ubiquitous on milkweeds in agricultural and ornamental settings, commonly encountered doses below 50 ng/g are unlikely to cause substantial declines in monarch survival or migratory performance.  more » « less
Award ID(s):
1754392
NSF-PAR ID:
10421016
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Insects
Volume:
12
Issue:
11
ISSN:
2075-4450
Page Range / eLocation ID:
999
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Numerous studies have documented the negative effects of neonicotinoids on bees; it remains crucial to examine how neonicotinoids affect other non‐target nectar‐feeding insects, such as the monarch butterfly,Danaus plexippus.

    Wildflowers growing near agricultural areas can be contaminated with neonicotinoids that affect survival or cause sublethal changes to behaviours of nectar‐feeding insects. Nectar residues of imidacloprid and clothianidin found in milkweeds and wildflowers adjacent to agricultural field range from 0 to 72.8 ng/mL.

    At field‐relevant doses, two neonicotinoids (imidacloprid and clothianidin) were studied for their effects on adult monarch survival, reproduction, flight and behaviour. First, we fed adult monarchs artificial nectar solutions ranging from 15 to 386 ng/mL of imidacloprid and 19 to 531 ng/mL of clothianidin. Neonicotinoid ingestion slightly reduced monarch reproduction but had no significant effects on survival, weight change, or activity levels.

    Second, we fed monarchs higher clothianidin doses (909 and 4030 ng/mL), that exceed field‐relevant levels by 22 and 99 times. These higher doses reduced monarch nectar consumption, survival, flight performance and reaction time in response to a drop test.

    Results show that adult monarchs tolerate field‐relevant doses as high as 54 ng/mL for imidacloprid and 75 ng/mL for clothianidin, with minimal lethal or sub‐lethal effects until much higher doses are supplied. We conclude that adult monarchs are more tolerant of ingested clothianidin and imidacloprid than indicated by previous research.

     
    more » « less
  2. Abstract

    Herbivorous insects have evolved many mechanisms to overcome plant chemical defences, including detoxification and sequestration. Herbivores may also use toxic plants to reduce parasite infection. Plant toxins could directly interfere with parasites or could enhance endogenous immunity. Alternatively, plant toxins could favour down‐regulation of endogenous immunity by providing an alternative (exogenous) defence against parasitism. However, studies on genomewide transcriptomic responses to plant defences and the interplay between plant toxicity and parasite infection remain rare. Monarch butterflies (Danaus plexippus) are specialist herbivores of milkweeds (Asclepiasspp.), which contain toxic cardenolides. Monarchs have adapted to cardenolides through multiple resistance mechanisms and can sequester cardenolides to defend against bird predators. In addition, high‐cardenolide milkweeds confer monarch resistance to a specialist protozoan parasite (Ophryocystis elektroscirrha). We used this system to study the interplay between the effects of plant toxicity and parasite infection on global gene expression. We compared transcriptional profiles between parasite‐infected and uninfected monarch larvae reared on two milkweed species. Our results demonstrate that monarch differentially express several hundred genes when feeding onA. curassavicaandA. incarnata, two species that differ substantially in cardenolide concentrations. These differentially expressed genes include genes within multiple families of canonical insect detoxification genes, suggesting that they play a role in monarch toxin resistance and sequestration. Interestingly, we found little transcriptional response to infection. However, parasite growth was reduced in monarchs reared onA. curassavica, and in these monarchs, several immune genes were down‐regulated, consistent with the hypothesis that medicinal plants can reduce reliance on endogenous immunity.

     
    more » « less
  3. Abstract

    Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterfliesDanaus plexippus, consistently experience infection by a virulent parasiteOphryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.

    We investigated plant‐mediated influences of elevated CO2(eCO2) on endogenous immune responses of monarch larvae to infection byO. elektroscirrha. Recently, transcriptomics have revealed that infection byO. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2alter the balance between exogenous and endogenous sources of immunity remains unknown.

    We fed monarchs two species of milkweed;A. curassavica(medicinal) andA. incarnata(non‐medicinal) grown under ambient CO2(aCO2) or eCO2. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.

    The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection byO. elektroscirrhawere generally lower in larvae reared on foliage from aCO2plants and higher in larvae reared on foliage from eCO2plants. When grown under eCO2, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2results in increased endogenous immune function.

    Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.

     
    more » « less
  4. Abstract

    Few studies have described the effects of larval diet quality on adult insect flight performance. Flight muscle development and high‐powered flight in insects are associated with costly energetic demands. Because larval diet is the energy source that powers these mechanisms, we asked whether larval diet has an impact on flight performance and metabolism in the monarch butterfly (Danaus plexippusLinnaeus).

    Monarch caterpillars from the eastern North American and Puerto Rican populations were fed a diet of eitherAsclepias incarnataL. (native to the eastern North American population) orAsclepias curassavicaL. (native to the Puerto Rican population and uncommon in eastern North America). We flew the monarchs on a tethered flight mill to acquire flight performance metrics including velocity, distance, duration, power, and oxygen consumption rate.

    Monarchs reared on theA. incarnata L. milkweed showed slower, shorter, and less powerful flights than those fed onA. curassavicaL. However, eastern North American and Puerto Rican monarchs, which were reared under summer conditions, did not differ in flight metrics or post‐flight metabolic rates.

    The results suggest that flight in eastern North American and Puerto Rican monarchs is similar during the breeding season, yet the milkweed the caterpillars consume has important implications for flight performance.

     
    more » « less
  5. Abstract

    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.

     
    more » « less