Anthropogenic Zinc Exposure Increases Mortality and Antioxidant Gene Expression in Monarch Butterflies with Low Access to Dietary Macronutrients.
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ABSTRACT:
SUBMITTER: Shephard AM
PROVIDER: S-EPMC9314993 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC8623494 | biostudies-literature
Project description:BackgroundNorth 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.MethodsHere, 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.ResultsWe 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.ConclusionsOur 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.
| S-EPMC6724006 | biostudies-literature
Project description:Insects are well known for their ability to keep track of their heading direction based on a combination of skylight cues and visual landmarks. This allows them to navigate back to their nest, disperse throughout unfamiliar environments, as well as migrate over large distances between their breeding and non-breeding habitats. The monarch butterfly (Danaus plexippus), for instance, is known for its annual southward migration from North America to certain trees in Central Mexico. To maintain a constant flight route, these butterflies use a time-compensated sun compass, which is processed in a region in the brain, termed the central complex. However, to successfully complete their journey, the butterflies' brain must generate a multitude of orientation strategies, allowing them to dynamically switch from sun-compass orientation to a tactic behavior toward a certain target. To study whether monarch butterflies exhibit different orientation modes and if they can switch between them, we observed the orientation behavior of tethered flying butterflies in a flight simulator while presenting different visual cues to them. We found that the butterflies' behavior depended on the presented visual stimulus. Thus, while a dark stripe was used for flight stabilization, a bright stripe was fixated by the butterflies in their frontal visual field. If we replaced a bright stripe with a simulated sun stimulus, the butterflies switched their behavior and exhibited compass orientation. Taken together, our data show that monarch butterflies rely on and switch between different orientation modes, allowing the animal to adjust orientation to its actual behavioral demands.
| S-EPMC8918799 | biostudies-literature
Project description:The annual migration of the monarch butterfly Danaus plexippus is in peril. In an effort to aid population recovery, monarch enthusiasts across North America participate in a variety of conservation efforts, including captive rearing and release of monarch butterflies throughout the summer and autumn. However, the impact of captive breeding on monarchs remains an open question. Here, we show that captive breeding, both commercially and by summertime hobbyists, causes migratory behavior to be lost. Monarchs acquired commercially failed to orient south when reared outdoors in the autumn, unlike wild-caught North American monarchs, yet they did enter reproductive diapause. The commercial population was genetically highly divergent from wild-caught North American monarchs and had rounder forewings, similar to monarchs from nonmigratory populations. Furthermore, rearing wild-caught monarchs in an indoor environment mimicking natural migration-inducing conditions failed to elicit southward flight orientation. In fact, merely eclosing indoors after an otherwise complete lifecycle outdoors was enough to disrupt southern orientation. Our results provide a window into the complexity-and remarkable fragility-of migration.
| S-EPMC6642386 | biostudies-literature
Project description:Given the rapid population decline and recent petition for listing of the monarch butterfly (Danaus plexippus L.) under the Endangered Species Act, an accurate estimate of the Eastern, migratory population size is needed. Because of difficulty in counting individual monarchs, the number of hectares occupied by monarchs in the overwintering area is commonly used as a proxy for population size, which is then multiplied by the density of individuals per hectare to estimate population size. There is, however, considerable variation in published estimates of overwintering density, ranging from 6.9-60.9 million ha-1. We develop a probability distribution for overwinter density of monarch butterflies from six published density estimates. The mean density among the mixture of the six published estimates was ?27.9 million butterflies ha-1 (95% CI [2.4-80.7] million ha-1); the mixture distribution is approximately log-normal, and as such is better represented by the median (21.1 million butterflies ha-1). Based upon assumptions regarding the number of milkweed needed to support monarchs, the amount of milkweed (Asclepias spp.) lost (0.86 billion stems) in the northern US plus the amount of milkweed remaining (1.34 billion stems), we estimate >1.8 billion stems is needed to return monarchs to an average population size of 6 ha. Considerable uncertainty exists in this required amount of milkweed because of the considerable uncertainty occurring in overwinter density estimates. Nevertheless, the estimate is on the same order as other published estimates. The studies included in our synthesis differ substantially by year, location, method, and measures of precision. A better understanding of the factors influencing overwintering density across space and time would be valuable for increasing the precision of conservation recommendations.
| S-EPMC5408724 | biostudies-literature
Project description:In the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. In contrast to spring and summer butterflies, fall migrants are juvenile hormone deficient, which leads to reproductive arrest and increased longevity. Migrants also use a time-compensated sun compass to help them navigate in the south/southwesterly direction en route for Mexico. Central issues in this area are defining the relationship between juvenile hormone status and oriented flight, critical features that differentiate summer monarchs from fall migrants, and identifying molecular correlates of behavioral state. Here we show that increasing juvenile hormone activity to induce summer-like reproductive development in fall migrants does not alter directional flight behavior or its time-compensated orientation, as monitored in a flight simulator. Reproductive summer butterflies, in contrast, uniformly fail to exhibit directional, oriented flight. To define molecular correlates of behavioral state, we used microarray analysis of 9417 unique cDNA sequences. Gene expression profiles reveal a suite of 40 genes whose differential expression in brain correlates with oriented flight behavior in individual migrants, independent of juvenile hormone activity, thereby separating molecularly fall migrants from summer butterflies. Intriguing genes that are differentially regulated include the clock gene vrille and the locomotion-relevant tyramine beta hydroxylase gene. In addition, several differentially regulated genes (37.5% of total) are not annotated, suggesting unique functions associated with oriented flight behavior. We also identified 23 juvenile hormone-dependent genes in brain, which separate reproductive from non-reproductive monarchs; genes involved in longevity, fatty acid metabolism, and innate immunity are upregulated in non-reproductive (juvenile-hormone deficient) migrants. The results link key behavioral traits with gene expression profiles in brain that differentiate migratory from summer butterflies and thus show that seasonal changes in genomic function help define the migratory state.
2009-01-01 | GSE14041 | GEO
Project description:In the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. In contrast to spring and summer butterflies, fall migrants are juvenile hormone deficient, which leads to reproductive arrest and increased longevity. Migrants also use a time-compensated sun compass to help them navigate in the south/southwesterly direction en route for Mexico. Central issues in this area are defining the relationship between juvenile hormone status and oriented flight, critical features that differentiate summer monarchs from fall migrants, and identifying molecular correlates of behavioral state. Here we show that increasing juvenile hormone activity to induce summer-like reproductive development in fall migrants does not alter directional flight behavior or its time-compensated orientation, as monitored in a flight simulator. Reproductive summer butterflies, in contrast, uniformly fail to exhibit directional, oriented flight. To define molecular correlates of behavioral state, we used microarray analysis of 9417 unique cDNA sequences. Gene expression profiles reveal a suite of 40 genes whose differential expression in brain correlates with oriented flight behavior in individual migrants, independent of juvenile hormone activity, thereby separating molecularly fall migrants from summer butterflies. Intriguing genes that are differentially regulated include the clock gene vrille and the locomotion-relevant tyramine beta hydroxylase gene. In addition, several differentially regulated genes (37.5% of total) are not annotated, suggesting unique functions associated with oriented flight behavior. We also identified 23 juvenile hormone-dependent genes in brain, which separate reproductive from non-reproductive monarchs; genes involved in longevity, fatty acid metabolism, and innate immunity are upregulated in non-reproductive (juvenile-hormone deficient) migrants. The results link key behavioral traits with gene expression profiles in brain that differentiate migratory from summer butterflies and thus show that seasonal changes in genomic function help define the migratory state. A total of 40 monarch butterflies were used for the microarray analysis. Of the 40, 10 (5 male/5 female) were summer butterflies (Designated as S) and 30 were fall butterflies. The fall butterflies were further divided into three groups: 10 (5 male/5 female) were untreated (F); 10 (5 male/5 female) were treated with methoprene (M), which is a juvenile hormone analog and induces the development of reproductive organs in migrant butterflies; and 10 (5 male/5 female) were treated with vehicle only (V). We collected total brain RNA from each of the 40 butterflies. The brain RNAs were amplified and then used to probe a custom Nimblegen array that was designed to analyze the 9,417 unique cDNA sequences established in our published EST library (http://titan.biotec.uiuc.edu/cgi-bin/ESTWebsite/estima_start?seqSet=butterfly). Our main interest is to find genes involved in migration. This includes genes regulating oriented flight behavior of the butterfly and genes that regulate reproductive status. To identify these genes, we approached the microarray data in two ways. First, we identified the potential genes involved in oriented flight behavior using the following strategy. We compared the summer group to each of the three fall groups (untreated, methoprene-treated, and vehicle-treated) for males and for females, and looked for gene regulation patterns common among the three comparisons for each sex. Because the comparisons were done separately for males and females, and our behavioral data did not show significant sex differences in flight orientation, we focused on the common differentially regulated genes that were shared between males and females. Accordingly, we identified 40 cDNAs that were differentially regulated between summer butterflies and fall migrants, irrespective of sex. Second, we looked for the juvenile hormone-response genes. Again, we performed sex-specific statistical analyses, and compared the summer and the fall groups, and the methoprene-treated and vehicle-treated migrants. We then screened for shared genes between the two groups for each sex. We next examined cDNAs that were differentially regulated in both males and females, to determine juvenile hormone-regulated genes involved in more global processes (e.g., longevity and fatty acid metabolism) that would not be expected to be sex-specific. We identified 23 putative juvenile hormone-response genes that were common between males and females.
2008-12-31 | E-GEOD-14041 | biostudies-arrayexpress
Project description:Many animals use the Earth's geomagnetic field for orientation and navigation. Yet, the molecular and cellular underpinnings of the magnetic sense remain largely unknown. A biophysical model proposed that magnetoreception can be achieved through quantum effects of magnetically-sensitive radical pairs formed by the photoexcitation of cryptochrome (CRY) proteins. Studies in Drosophila are the only ones to date to have provided compelling evidence for the ultraviolet (UV)-A/blue light-sensitive type 1 CRY (CRY1) involvement in animal magnetoreception, and surprisingly extended this discovery to the light-insensitive mammalian-like type 2 CRYs (CRY2s) of both monarchs and humans. Here, we show that monarchs respond to a reversal of the inclination of the Earth's magnetic field in an UV-A/blue light and CRY1, but not CRY2, dependent manner. We further demonstrate that both antennae and eyes, which express CRY1, are magnetosensory organs. Our work argues that only light-sensitive CRYs function in animal light-dependent inclination-based magnetic sensing.
| S-EPMC7859408 | biostudies-literature
Project description:Human activities are increasing the environmental availability of micronutrients, including sodium and some essential metals. Micronutrients are often limiting in animal diets but may have negative effects when consumed in excess. Though prior research has documented how elevated exposure to individual micronutrients can impact organismal development and fitness, we know less about combined effects of multiple micronutrients. In the wild, monarch butterfly larvae (Danaus plexippus) commonly consume plants in roadside habitats that contain elevated levels of sodium (from road salt) and zinc (from vehicle wear-and-tear). We reared monarch caterpillars to adulthood to test individual and combined effects of dietary sodium and zinc on components of fitness, sodium-linked phenotypes (proxies for neural and flight muscle development) and concentrations of sodium and zinc in adult butterflies. Monarch survival was not impacted by elevated sodium or zinc individually or in combination. Yet, monarchs feeding on sodium-treated milkweed developed relatively larger eyes, consistent with a positive effect of sodium on neural development. Measurements of element concentrations in butterfly and plant tissue indicated that monarchs had higher zinc levels than those present in zinc-treated milkweed but lower sodium levels than those present in sodium-treated milkweed. Monarchs developing on sodium-treated milkweed also had prolonged development time, which might be a cost associated with developing extra neural tissue or investing in mechanisms to excrete excess dietary sodium during the larval stage. Our results indicate that sodium, more than zinc, is likely influencing phenotypic development and performance of insect pollinators in roadside habitats. Yet, in contrast to previous work, our experiment suggests that the highest levels of sodium found along roads are not always harmful for developing monarchs. Future work could consider how potentially stressful effects of micronutrients could be mitigated by increased macronutrient availability or how developmental factors such as migratory status might increase micronutrient requirements.
| S-EPMC8354372 | biostudies-literature
Project description:BackgroundIn the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. In contrast to spring and summer butterflies, fall migrants are juvenile hormone deficient, which leads to reproductive arrest and increased longevity. Migrants also use a time-compensated sun compass to help them navigate in the south/southwesterly direction en route for Mexico. Central issues in this area are defining the relationship between juvenile hormone status and oriented flight, critical features that differentiate summer monarchs from fall migrants, and identifying molecular correlates of behavioral state.ResultsHere we show that increasing juvenile hormone activity to induce summer-like reproductive development in fall migrants does not alter directional flight behavior or its time-compensated orientation, as monitored in a flight simulator. Reproductive summer butterflies, in contrast, uniformly fail to exhibit directional, oriented flight. To define molecular correlates of behavioral state, we used microarray analysis of 9417 unique cDNA sequences. Gene expression profiles reveal a suite of 40 genes whose differential expression in brain correlates with oriented flight behavior in individual migrants, independent of juvenile hormone activity, thereby molecularly separating fall migrants from summer butterflies. Intriguing genes that are differentially regulated include the clock gene vrille and the locomotion-relevant tyramine beta hydroxylase gene. In addition, several differentially regulated genes (37.5% of total) are not annotated. We also identified 23 juvenile hormone-dependent genes in brain, which separate reproductive from non-reproductive monarchs; genes involved in longevity, fatty acid metabolism, and innate immunity are upregulated in non-reproductive (juvenile-hormone deficient) migrants.ConclusionThe results link key behavioral traits with gene expression profiles in brain that differentiate migratory from summer butterflies and thus show that seasonal changes in genomic function help define the migratory state.
| S-EPMC2681450 | biostudies-literature