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
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
- PAR ID:
- 10421016
- 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
-
-
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
-
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 exposed 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.more » « less
-
Mansour, Ramzi (Ed.)The preference-performance hypothesis explains host specificity in phytophagous insects, positing that host plants chosen by adults confer the greatest larval fitness. However, adults sometimes oviposit on plants supporting low larval success because the components of host specificity (adult preference, plant palatability, and larval survival) are non-binary and not necessarily correlated. Palatability (willingness to eat) is governed by chemical cues and physical barriers such as trichomes, while survival (ability to complete development) depends upon nutrition and toxicity. Absence of a correlation between the components of host specificity results in low-performance hosts supporting limited larval development. Most studies of specificity focus on oviposition behavior leaving the importance and basis of palatability and survival under-explored. We conducted a comprehensive review of 127 plant species that have been claimed or tested to be hosts for the monarch butterfly Danaus plexippus to classify them as non-hosts, low performance, or high performance. We performed a meta-analysis to test if performance status could be explained by properties of neurotoxic cardenolides or trichome density. We also conducted a no-choice larval feeding experiment to identify causes of low performance. We identified 34 high performance, 42 low performance, 33 non-hosts, and 18 species with unsubstantiated claims. Mean cardenolide concentration was greater in high- than low-performance hosts and a significant predictor of host status, suggesting possible evolutionary trade-offs in monarch specialization. Other cardenolide properties and trichome density were not significant predictors of host status. In the experiment, we found, of the 62% of larvae that attempted to eat low-performance hosts, only 3.5% survived to adult compared to 85% of those on the high-performance host, demonstrating that multiple factors affect larval host plant specificity. Our study is the first to classify all known host plants for monarchs and has conservation implications for this threatened species.more » « less
-
1. Many migratory animals undergo physiological and behavioural changes to prepare for and sustain long‐distance movements. Because insect migrations are common and diverse, studies that examine how migratory insects meet the energetic demands of long‐distance movements are badly needed. 2. Monarch butterflies (Danaus plexippus) migrate up to 4000 km annually from eastern North America to wintering sites in central Mexico. Autumn generation monarchs undergo physiological and behavioural changes in response to environmental cues to initiate migration. In particular, exposure to cooler temperatures and shorter day lengths in early autumn causes monarchs to enter the hormonally induced state of reproductive diapause. 3. This study examined differences in flight‐associated metabolic rate (MR) and flight performance metrics for monarchs experimentally reared under autumn‐like conditions (typically experienced before the southward migration) relative to monarchs reared under summer‐like conditions. 4. Adult monarchs reared under autumn‐like conditions showed lower post‐flight MRs, greater flight efficiency, and lower measures of reproductive activity relative to monarchs reared under summer‐like conditions. Increases in post‐flight metabolism were associated with monarch body weight, age, and flight velocity. 5. These findings suggest that a trans‐generational shift in flight energetics is an important component of the monarch's complex migratory syndrome, and that physiological changes that accompany reproductive diapause facilitate energy conservation during flight.more » « less
An official website of the United States government

