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
Host plant specificity of the monarch butterfly Danaus plexippus: A systematic review and meta-analysis
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
- Award ID(s):
- 1754434
- PAR ID:
- 10383204
- Editor(s):
- Mansour, Ramzi
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 17
- Issue:
- 6
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0269701
- 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
-
null (Ed.)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 mean 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.more » « less
-
Variation in immune response in the generalist herbivore fall webworm across four common host plantsAbstract Dietary generalist herbivorous insects are widespread and often occur in a variety of environments. Across their geographic range, herbivorous insects may encounter variable plant traits as they feed on high‐quality or low‐quality plants. Herbivorous insect larvae experience both bottom‐up (host plant) and top‐down (parasitoid) factors that affect survival. Host plant quality may affect larval growth and survival in that larvae feeding on low‐quality plants often suffer reduced fitness. However, herbivores on different host plants are also subject to different levels of parasitism. High‐quality plants confer stronger larval performance (higher survival, more offspring), but larvae may also face higher parasitism. In some herbivore species, diet mediates larval immune response. The generalist insect herbivore fall webworm (FW),Hyphantria cuneaDrury (Lepidoptera: Erebidae), is a moth native to North America, and its larvae have considerable variance in their performance when reared on different host plants. We investigated whether diet affects the immune response in FW larvae when they are reared on different host plant species known to vary in food quality. We measured immune response by melanization of a nylon filament. We found significant differences in immune response across host plants, indicating that diet mediates immune response in FW larvae. Our study helps elucidate the factors that cause variation in immune response in a generalist herbivore.more » « less
-
Host shifts are considered a key generator of insect biodiversity. For insects, adaptation to new host plants often requires changes in larval/pupal development and adult behavioural preference toward new hosts. Neurochemicals play key roles in both development and behaviour and therefore provide a potential source for such synchronization. Here, we correlated life-history timing, brain development and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. These races exhibit differences in pupal diapause timing as well as adult behavioural preference with respect to their hosts. This difference in behavioural preference is coupled with differences in neurophysiological response to host volatiles. We found that apple race pupae exhibited adult brain morphogenesis three weeks faster after an identical simulated winter than the hawthorn race, which correlated with significantly lower titres of several neurochemicals. In some cases, particularly biogenic amines, differences in titres were reflected in the mature adult stage, when host preference is exhibited. In summary, life-history timing, neurochemical titre and brain development can be coupled in this speciating system, providing new hypotheses for the origins of new species through host shifts.more » « less
An official website of the United States government

