Monarchs Reared in Winter in California Are Not Large Enough to Be Migrants. Comment on James et al. First Population Study on Winter Breeding Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) in the Urban South Bay of San Francisco, California. Insects 2021, 12, 946

A recent study in this journal aimed to understand certain changes in the wintering behavior of monarch butterflies, specifically in the western subpopulation of North America [...]

Reply to Davis, A.K. Monarchs Reared in Winter in California Are Not Large Enough to Be Migrants. Comment on “James et al. First Population Study on Winter Breeding Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) in the Urban South Bay of San Francisco, California. Insects 2021, 12, 946”

This is a reply to the comment from Davis [...]

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.

Stimulus-dependent orientation strategies in monarch butterflies

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.

Population-specific patterns of toxin sequestration in monarch butterflies from around the world

Monarch butterflies are one of the preeminent examples of a toxin-sequestering animal, gaining protection against predators via cardenolides obtained from their milkweed host plants. Although cardenolide sequestration by monarchs has been studied in ecological, physiological, and phylogenetic contexts, relatively little research has surveyed genetic variation in the ability to sequester, nor has monarch sequestration been studied in relation to divergent host plant assemblages or variation in exposure to predation. Here, we use the monarch's recent global range expansion to test hypotheses about how cardenolide sequestration evolves over relatively contemporary time scales. First, we test for whether sympatric monarch/milkweed combinations have a sequestration advantage by rearing six geographically disparate monarch populations on six associated milkweed host species and measuring levels of sequestered cardenolides in a set of 440 adult butterflies. Second, we use monarchs from Guam - an oceanic island where birds have been functionally extirpated for approximately 40 years - to test hypotheses about how exposure to avian predation affects cardenolide sequestration. We find little overall evidence for increased sequestration on sympatric hosts. However, one monarch population (Puerto Rico) shows strong support for cross-host tradeoffs in sequestration ability, primarily driven by limited sequestration of polar cardenolides from two temperate North American milkweeds (Asclepias syriaca and A. speciosa). Monarchs from Guam show some evidence for reduced cardenolide sequestration in both a cross-island comparison of wild-caught butterflies as well as population-level comparisons of greenhouse-reared butterflies. Our results suggest that there is substantial genetic variation in sequestration ability (both within and between monarch populations) and that evolutionary history and contemporary species interactions may influence patterns of cardenolide sequestration.

Exploring the Role of Cognition in the Annual Fall Migration of the Monarch Butterfly (Danaus plexippus)

Each fall, monarch butterflies in eastern North America undergo an extraordinary long-distance migration to wintering areas in central Mexico, where they remain until returning northward in the spring. Migrants survive the overwintering period by metabolizing lipid reserves accumulated exclusively though floral nectar; however, there is little known about how individuals maximize foraging efficiency in the face of floral environments that constantly change in complex and unpredictable ways along their migratory route. Here, a proboscis extension paradigm is used to investigate the role of cognition during the foraging phase of monarch migration. Male and female migratory butterflies were consecutively trained to discriminate between two color and odor cues and then tested for their ability to simultaneously retain the information on the reward value of each cue in memory without reinforcement over a period of 7 days. To gain further insight into cognitive abilities of monarchs as a migratory species, a second set of captive-reared males and females were tested under harnessed conditions at the same time as wild-caught fall migrants. Results showed that male and female migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies, as a migratory species, have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation.

No broad decline of breeding monarch butterflies in North America: implications for conservation efforts

Many insects are in clear decline, with monarch butterflies (Danaus plexippus) drawing particular attention as a flagship species. Falling numbers of overwintering monarchs are well documented, but there has been debate regarding population trends of summer breeding populations. Here, we compile a series of long-term monarch monitoring datasets, some which are analyzed here for the first time, that reveal highly variable responses across the migratory geographic range, but no broad net decline in numbers of breeding monarchs. We also did not find evidence that sampling biased towards natural sites was masking declines at disturbed sites. Overall, our results suggest a robust resiliency in summer populations that thus far has allowed recovery from losses during the winter. Thus, monarchs may not require as much breeding habitat restoration as once thought, and focus should be on conserving the fall and spring migration.