scholarly journals Effects of early-life exposure to sublethal levels of a common neonicotinoid insecticide on the orientation and migration of monarch butterflies (Danaus plexippus)

2020 ◽  
Vol 224 (4) ◽  
pp. jeb230870
Author(s):  
Alana A. E. Wilcox ◽  
Amy E. M. Newman ◽  
Nigel E. Raine ◽  
Greg W. Mitchell ◽  
D. Ryan Norris

ABSTRACTMigratory insects use a variety of innate mechanisms to determine their orientation and maintain correct bearing. For long-distance migrants, such as the monarch butterfly (Danaus plexippus), these journeys could be affected by exposure to environmental contaminants. Neonicotinoids are synthetic insecticides that work by affecting the nervous system of insects, resulting in impairment of their mobility, cognitive performance, and other physiological and behavioural functions. To examine how neonicotinoids might affect the ability of monarch butterflies to maintain a proper directional orientation on their ∼4000 km migration, we grew swamp milkweed (Asclepias incarnata) in soil that was either untreated (0 ng g−1: control) or mixed with low (15 ng g−1 of soil) or high (25 ng g−1 of soil) levels of the neonicotinoid clothianidin. Monarch caterpillars were raised on control or clothianidin-treated milkweed and, after pupation, either tested for orientation in a static flight simulator or radio-tracked in the wild during the autumn migration period. Despite clothianidin being detectable in milkweed tissue consumed by caterpillars, there was no evidence that clothianidin influenced the orientation, vector strength (i.e. concentration of direction data around the mean) or rate of travel of adult butterflies, nor was there evidence that morphological traits (i.e. mass and forewing length), testing time, wind speed or temperature impacted directionality. Although sample sizes for both flight simulator and radio-tracking tests were limited, our preliminary results suggest that clothianidin exposure during early caterpillar development does not affect the directed flight of adult migratory monarch butterflies or influence their orientation at the beginning of migration.

2020 ◽  
Author(s):  
Alana A. E. Wilcox ◽  
Amy E. M. Newman ◽  
Nigel E. Raine ◽  
D. Ryan Norris

AbstractEastern North American migratory monarch butterflies (Danaus plexippus) have faced sharp declines over the last two decades. Although captive rearing has been used as an important tool for engaging the public and supplementing conservation efforts, a recent study that tested monarchs in a flight simulator suggested that captive-reared monarchs lose their capacity to orient southward during fall migration to their Mexican overwintering sites. We raised offspring of wild-caught monarchs on swamp milkweed (Asclepias incarnata) and, after eclosion, individuals were either tested in a flight simulator or radio-tracked in the wild using array of over 100 automated telemetry towers. While only 33% (7/39) of monarchs tested in the flight simulator showed strong southeast to southwest orientation, 97% (28/29) of the radio-tracked individuals were detected by automated towers south or southeast of the release site, up to 200 km away. Our results suggest that, though captive rearing of monarch butterflies may cause temporary disorientation, proper orientation is likely re-established after exposure to natural skylight cues.


2020 ◽  
Vol 16 (4) ◽  
pp. 20190922 ◽  
Author(s):  
Andrew K. Davis ◽  
Farran M. Smith ◽  
Ashley M. Ballew

For many animals and insects that are experiencing dramatic population declines, the only recourse for conservationists is captive rearing. To ensure success, reared individuals should be biologically indistinct from those in the wild. We tested if this is true with monarch butterflies, Danaus plexippus , which are increasingly being reared for release by citizens and commercial breeders. Since late-summer monarchs should be as migration capable as possible for surviving the arduous long-distance migration, we evaluated four migration-relevant traits across two groups of captive-reared monarchs ( n = 41 and 42) and one group of wild-caught migrants ( n = 41). Monarchs (descendants of wild individuals) were reared from eggs to adulthood either in a warm indoor room next to a window, or in an incubator that mimicked late-summer conditions. Using an apparatus consisting of a perch mounted to an electronic force gauge, we assessed ‘grip strength' of all groups, then used image analysis to measure forewing size, pigmentation and elongation. In three of the four traits, reared monarchs underperformed compared to wild ones, even those reared under conditions that should have produced migration-ready individuals. The average strength of reared monarchs combined was 56% less than the wild group, even when accounting for size. Their orange wing colour was paler (an indicator of poor condition and flight ability) and their forewings were less elongated (elongation is associated with migration propensity) than wild monarchs. The reason(s) behind these effects is unknown but could stem from the frequent disturbance and/or handling of reared monarchs, or the fact that rearing removes the element of natural selection from all stages. Regardless, these results explain prior tagging studies that showed reared monarchs have lower migratory success compared to wild.


2020 ◽  
Author(s):  
Patrick Anthony Guerra ◽  
Stephen Matter

Abstract BackgroundIndividuals of many species that perform annual long-distance migrations are capable of stopping at specific overwintering destinations, despite having not been there before. The iconic monarch butterfly (Danaus plexippus) and its annual long-distance fall migration is a famous example of this phenomenon. During the fall, Eastern North American monarch butterflies use various compass mechanisms to properly orient their flight southwards, in order to leave their summer breeding grounds in Southern Canada and the Northern United States, and reach their overwintering sites in Central Mexico. It remains a mystery, however, how monarchs locate and stop at these specific, consistent overwintering sites, especially since these individuals are on their maiden voyage. MethodsWe test the hypothesis that fall migrant monarchs locate these overwintering sites by using an innate, inherited map sense based on sensing and responding to specific geomagnetic signatures that are correlated with the overwintering sites. Using a natural displacement approach, we examined if the locations of overwintering sites and the abundance of monarchs at them, changes with the natural shift of the Earth’s magnetic field over time (2004-2018).ResultsWe found that despite the natural displacement of the geomagnetic field over the years, the locations of the overwintering sites and monarch abundance were unaffected. For example, fall monarchs continued to overwinter at the most southern sites in Mexico, even when the geomagnetic coordinates associated with these sites would have shifted north due to the natural shift of the Earth’s magnetic field, placing these sites significantly outside the range of the overwintering area.ConclusionsOur results suggest that monarchs do not employ a map sense based on geomagnetic cues for finding their overwintering sites, and might instead use other mechanisms or strategies for locating them (potentially using localized sensory cues) once they are near or have arrived in Central Mexico. We suggest that future work should now focus on understanding what these cue parameters are, in order to inform conservation efforts that are aimed at protecting the threatened monarch butterfly and preserving its annual long-distance migration.


2020 ◽  
Vol 117 (46) ◽  
pp. 28887-28893
Author(s):  
Micah G. Freedman ◽  
Hugh Dingle ◽  
Sharon Y. Strauss ◽  
Santiago R. Ramírez

Migratory animals exhibit traits that allow them to exploit seasonally variable habitats. In environments where migration is no longer beneficial, such as oceanic islands, migration-association traits may be selected against or be under relaxed selection. Monarch butterflies are best known for their continent-scale migration in North America but have repeatedly become established as nonmigrants in the tropical Americas and on Atlantic and Pacific Islands. These replicated nonmigratory populations provide natural laboratories for understanding the rate of evolution of migration-associated traits. We measured >6,000 museum specimens of monarch butterflies collected from 1856 to the present as well as contemporary wild-caught monarchs from around the world. We determined 1) how wing morphology varies across the monarch’s global range, 2) whether initial long-distance founders were particularly suited for migration, and 3) whether recently established nonmigrants show evidence for contemporary phenotypic evolution. We further reared >1,000 monarchs from six populations around the world under controlled conditions and measured migration-associated traits. Historical specimens show that 1) initial founders are well suited for long-distance movement and 2) loss of seasonal migration is associated with reductions in forewing size and elongation. Monarch butterflies raised in a common garden from four derived nonmigratory populations exhibit genetically based reductions in forewing size, consistent with a previous study. Our findings provide a compelling example of how migration-associated traits may be favored during the early stages of range expansion, and also the rate of reductions in those same traits upon loss of migration.


2021 ◽  
Author(s):  
Myriam Franzke ◽  
Christian Kraus ◽  
Maria Gayler ◽  
David Dreyer ◽  
Keram Pfeiffer ◽  
...  

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 for orientation 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 if 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 by a simulated sun stimulus, the butterflies switched their orientation behavior and exhibited compass orientation. Taken together, our data show that monarch butterflies rely on and switch between different orientation modes, allowing them to adjust orientation to the actual behavioral demands of the animal.


FACETS ◽  
2019 ◽  
Vol 4 (1) ◽  
pp. 238-253
Author(s):  
D. T. Tyler Flockhart ◽  
Maxim Larrivée ◽  
Kathleen L. Prudic ◽  
D. Ryan Norris

Monarch butterflies ( Danaus plexippus, Linnaeus, 1758) are comprised of two migratory populations separated by the Rocky Mountains and are renowned for their long-distance movements among the United States, Canada, and Mexico. Both populations have declined over several decades across North America prompting all three countries to evaluate conservation efforts. Monitoring monarch distribution and abundance is a necessary aspect of ongoing management in Canada where they are a species at risk. We used presence-only data from two citizen science data sets to estimate the annual breeding distribution of monarch butterflies in Canada between 2000 and 2015. Monarch breeding distribution in Canada varied widely among years owing to natural variation, and when considering the upper 95% of the probability of occurrence, the annual mean breeding distribution in Canada was 484 943 km2 (min: 173 449 km2; max: 1 425 835 km2). The area of occurrence was approximately an order of magnitude larger in eastern Canada than in western Canada. Habitat restoration for monarch butterflies in Canada should prioritize productive habitats in southern Ontario where monarchs occur annually and, therefore, likely contribute most to the long-term viability of monarchs in eastern North America. Overall, our assessment sets the geographic context to develop successful management strategies for monarchs in Canada.


2019 ◽  
Vol 116 (29) ◽  
pp. 14671-14676 ◽  
Author(s):  
Ayşe Tenger-Trolander ◽  
Wei Lu ◽  
Michelle Noyes ◽  
Marcus R. Kronforst

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.


2014 ◽  
Vol 2 (1) ◽  
Author(s):  
Dara A. Satterfield ◽  
Andrew K. Davis

AbstractThe migration of monarch butterflies (Danaus plexippus) in North America has a number of parallels with long-distance bird migration, including the fact that migratory populations of monarchs have larger and more elongated forewings than residents. These characteristics likely serve to optimize flight performance in monarchs, as they also do with birds. A question that has rarely been addressed thus far in birds or monarchs is if and how wing characteristics vary within a migration season. Individuals with superior flight performance should migrate quickly, and/or with minimal stopovers, and these individuals should be at the forefront of the migratory cohort. Conversely, individuals with poor flight performance and/or low endurance would be more likely to fall behind, and these would comprise the latest migrants. Here we examined how the wing morphology of migrating monarchs varies to determine if wing characteristics of early migrants differ from late migrants. We measured forewing area, elongation (length/width), and redness, which has been shown to predict flight endurance in monarchs. Based on a collection of 75 monarchs made one entire season (fall 2010), results showed that the earliest migrants (n = 20) in this cohort had significantly redder and more elongated forewings than the latest migrants (n = 17). There was also a non-significant tendency for early migrants to have larger forewing areas. These results suggest that the pace of migration in monarchs is at least partly dependent on the properties of their wings. Moreover, these data also raise a number of questions about the ultimate fate of monarchs that fall behind


2021 ◽  
Author(s):  
M. Jerome Beetz ◽  
Christian Kraus ◽  
Myriam Franzke ◽  
David Dreyer ◽  
Martin F. Strube-Bloss ◽  
...  

AbstractHead direction can be represented in a self-centered egocentric or a viewpoint-invariant allocentric reference frame. Using the most efficient representation is especially crucial for migrating animals, like monarch butterflies (Danaus plexippus) that use the sun for orientation. With tetrode recordings from the brain of tethered flying monarch butterflies, we examined the reference frame in which insects encode heading. We show that compass neurons switch their reference frame in a state-dependent manner. In quiescence, they encode sun-bearing angles, allowing the butterfly to map the environment within an egocentric frame. However, during flight, the same neurons encode heading within an allocentric frame. This switch converts the sun from a local to a global cue, an ideal strategy for maintaining a migratory heading over large distance.One-Sentence SummaryHeading information is encoded in different state-dependent reference frames in the monarch butterfly central complex


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