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, 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.
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,
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.
- Award ID(s):
- NSF-PAR ID:
- Publisher / Repository:
- Date Published:
- Journal Name:
- Ecological Entomology
- Page Range / eLocation ID:
- p. 531-543
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
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
Insect–pathogen dynamics can show seasonal and inter‐annual variations that covary with fluctuations in insect abundance and climate. Long‐term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence.
Danaus plexippusare commonly infected with the protozoan Ophryocystis elektroscirrha( OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection.
Here we compiled data on
OEinfection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration.
Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid‐2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result of
OE, highlighting the need to consider the parasite as a potential threat to the monarch population.
Increases in infection among eastern North American monarchs post‐2002 suggest that changes to the host’s ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.
Long-distance flight is crucial for the survival of migratory insects, and disruptions to their flight capacity can have significant consequences for conservation. In this study, we examined how a widely used insecticide, clothianidin (class: neonicotinoid), impacted the flight performance of two species of migratory butterflies, monarchs (Danaus plexippus) and painted ladies (Vanessa cardui). To do this, we quantified the free-flight energetics and tethered-flight velocity and distance of the two species using flow-through respirometry and flight mill assays. Our findings show differential effects of the pesticide on the two species. For painted ladies, we found that clothianidin exposure reduced average free-flight metabolic rates, but did not affect either average velocity or total distance during tethered flight. Other studies have linked low flight metabolic rates with reduced dispersal capacity, indicating that clothianidin exposure may hinder painted lady flight performance in the wild. Conversely, for monarchs, we saw no significant effect of clothianidin exposure on average free-flight metabolic rates but did observe increases in the average velocity, and for large individuals, total distance achieved by clothianidin-exposed monarchs in tethered flight. This suggests a potential stimulatory response of monarchs to low-dose exposures to clothianidin. These findings indicate that clothianidin exposure has the potential to influence the flight performance of butterflies, but that not all species are impacted in the same way. This highlights the need to be thoughtful when selecting performance assays, as different assays can evaluate fundamentally distinct aspects of physiology, and as such may yield divergent results.
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 butterflies
Danaus plexippus, consistently experience infection by a virulent parasite Ophryocystis 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 by
O. elektroscirrha. Recently, transcriptomics have revealed that infection by O. 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) and A. 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 by
O. 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.
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.