Changes in climate drive recent monarch butterfly dynamics.

Declines in the abundance and diversity of insects pose a substantial threat to terrestrial ecosystems worldwide. Yet, identifying the causes of these declines has proved difficult, even for well-studied species like monarch butterflies, whose eastern North American population has decreased markedly over the last three decades. Three hypotheses have been proposed to explain the changes observed in the eastern monarch population: loss of milkweed host plants from increased herbicide use, mortality during autumn migration and/or early-winter resettlement and changes in breeding-season climate. Here, we use a hierarchical modelling approach, combining data from >18,000 systematic surveys to evaluate support for each of these hypotheses over a 25-yr period. Between 2004 and 2018, breeding-season weather was nearly seven times more important than other factors in explaining variation in summer population size, which was positively associated with the size of the subsequent overwintering population. Although data limitations prevent definitive evaluation of the factors governing population size between 1994 and 2003 (the period of the steepest monarch decline coinciding with a widespread increase in herbicide use), breeding-season weather was similarly identified as an important driver of monarch population size. If observed changes in spring and summer climate continue, portions of the current breeding range may become inhospitable for monarchs. Our results highlight the increasingly important contribution of a changing climate to insect declines.

Traffic influences nutritional quality of roadside plants for monarch caterpillars.

Roadside habitats are increasingly being targeted for restoration and conservation. Roadside habitats often exhibit altered soil and plant chemistry due to pollution from maintenance (e.g. de-icing salt), car deterioration, and exhaust. Roadside plants may attract animals due to elevated levels of sodium or nitrogen, but high concentrations of heavy metals and sodium can be toxic, potentially setting an ecological trap. In this study, we determine how roads influence the chemistry of common milkweed (Asclepias syriaca) as it is the primary roadside host plant for the declining monarch butterfly (Danaus plexippus) in the eastern United States. Even though road salt is applied during the winter, we detect enhanced sodium along roads the following growing season. Road salts increase soil sodium, which in turn elevates host-plant foliar sodium (occasionally to toxic levels in <10% of plants) and sodium content in monarch caterpillars feeding on these plants. Sodium levels of milkweed leaves are highest close to the edge of busy roads. Some heavy metals (lead, zinc) are also elevated in roadside soils or plants. Nitrogen content was affected by adjacent agricultural use, but not traffic volume or proximity to a road. Other potential road pollutants (e.g. nickel) were not elevated in soil or plants. Despite a clear signature of road pollution in the chemistry of milkweed, most plants are likely still suitable for developing monarchs. Nonetheless, restoration investments in snowy regions should prioritize sites with lower-traffic density that are further from the road edge to minimize toxic impacts of high sodium. To extend this research to other insects of conservation concern, future work should characterize the nutritional quality of nectar, pollen, and other species of host-plants in roadside habitats.

Monarchs in decline: a collateral landscape-level effect of modern agriculture.

We review the postulated threatening processes that may have affected the decline in the eastern population of the monarch butterfly, Danaus plexippus L. (Lepidoptera: Nymphalidae), in North America. Although there are likely multiple contributing factors, such as climate and resource-related effects on breeding, migrating, and overwintering populations, the key landscape-level change appears to be associated with the widespread use of genetically modified herbicide resistant crops that have rapidly come to dominate the extensive core summer breeding range. We dismiss misinterpretations of the apparent lack of population change in summer adult count data as logically flawed. Glyphosate-tolerant soybean and maize have enabled the extensive use of this herbicide, generating widespread losses of milkweed (Asclepias spp.), the only host plants for monarch larvae. Modeling studies that simulate lifetime realized fecundity at a landscape scale, direct counts of milkweeds, and extensive citizen science data across the breeding range suggest that a herbicide-induced, landscape-level reduction in milkweed has precipitated the decline in monarchs. A recovery will likely require a monumental effort for the re-establishment of milkweed resources at a commensurate landscape scale.

Interpreting surveys to estimate the size of the monarch butterfly population: Pitfalls and prospects.

To assess the change in the size of the eastern North American monarch butterfly summer population, studies have used long-term data sets of counts of adult butterflies or eggs per milkweed stem. Despite the observed decline in the monarch population as measured at overwintering sites in Mexico, these studies found no decline in summer counts in the Midwest, the core of the summer breeding range, leading to a suggestion that the cause of the monarch population decline is not the loss of Midwest agricultural milkweeds but increased mortality during the fall migration. Using these counts to estimate population size, however, does not account for the shift of monarch activity from agricultural fields to non-agricultural sites over the past 20 years, as a result of the loss of agricultural milkweeds due to the near-ubiquitous use of glyphosate herbicides. We present the counter-hypotheses that the proportion of the monarch population present in non-agricultural habitats, where counts are made, has increased and that counts reflect both population size and the proportion of the population observed. We use data on the historical change in the proportion of milkweeds, and thus monarch activity, in agricultural fields and non-agricultural habitats to show why using counts can produce misleading conclusions about population size. We then separate out the shifting proportion effect from the counts to estimate the population size and show that these corrected summer monarch counts show a decline over time and are correlated with the size of the overwintering population. In addition, we present evidence against the hypothesis of increased mortality during migration. The milkweed limitation hypothesis for monarch decline remains supported and conservation efforts focusing on adding milkweeds to the landscape in the summer breeding region have a sound scientific basis.

Quasi-extinction risk and population targets for the Eastern, migratory population of monarch butterflies (Danaus plexippus).

The Eastern, migratory population of monarch butterflies (Danaus plexippus), an iconic North American insect, has declined by ~80% over the last decade. The monarch's multi-generational migration between overwintering grounds in central Mexico and the summer breeding grounds in the northern U.S. and southern Canada is celebrated in all three countries and creates shared management responsibilities across North America. Here we present a novel Bayesian multivariate auto-regressive state-space model to assess quasi-extinction risk and aid in the establishment of a target population size for monarch conservation planning. We find that, given a range of plausible quasi-extinction thresholds, the population has a substantial probability of quasi-extinction, from 11-57% over 20 years, although uncertainty in these estimates is large. Exceptionally high population stochasticity, declining numbers, and a small current population size act in concert to drive this risk. An approximately 5-fold increase of the monarch population size (relative to the winter of 2014-15) is necessary to halve the current risk of quasi-extinction across all thresholds considered. Conserving the monarch migration thus requires active management to reverse population declines, and the establishment of an ambitious target population size goal to buffer against future environmentally driven variability.

Tracking climate impacts on the migratory monarch butterfly.

Understanding the impacts of climate on migratory species is complicated by the fact that these species travel through several climates that may be changing in diverse ways throughout their complete migratory cycle. Most studies are not designed to tease out the direct and indirect effects of climate at various stages along the migration route. We assess the impacts of spring and summer climate conditions on breeding monarch butterflies, a species that completes its annual migration cycle over several generations. No single, broad-scale climate metric can explain summer breeding phenology or the substantial year-to-year fluctuations observed in population abundances. As such, we built a Poisson regression model to help explain annual arrival times and abundances in the Midwestern United States. We incorporated the climate conditions experienced both during a spring migration/breeding phase in Texas as well as during subsequent arrival and breeding during the main recruitment period in Ohio. Using data from a state-wide butterfly monitoring network in Ohio, our results suggest that climate acts in conflicting ways during the spring and summer seasons. High spring precipitation in Texas is associated with the largest annual population growth in Ohio and the earliest arrival to the summer breeding ground, as are intermediate spring temperatures in Texas. On the other hand, the timing of monarch arrivals to the summer breeding grounds is not affected by climate conditions within Ohio. Once in Ohio for summer breeding, precipitation has minimal impacts on overall abundances, whereas warmer summer temperatures are generally associated with the highest expected abundances, yet this effect is mitigated by the average seasonal temperature of each location in that the warmest sites receive no benefit of above average summer temperatures. Our results highlight the complex relationship between climate and performance for a migrating species and suggest that attempts to understand how monarchs will be affected by future climate conditions will be challenging.

Monarch butterfly migration and parasite transmission in eastern North America.

Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies (Danaus plexippus) and a protozoan parasite (Ophryocystis elektroscirrha) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long-distance migration weeds out infected animals (i.e., migratory culling). We combined field-sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within-breeding-season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.

Impacts of ultra-low volume resmethrin applications on non-target insects.

We studied the impacts of exposure to ultra-low volume (ULV) applications of resmethrin (Scourge) on monarch butterfly (Danaus plexippus) larvae and adults. In a series of 3 experiments, we measured short- and long-term survival of monarch larvae and adults, and the impacts of consuming previously exposed host plants on monarch larvae. We measured efficacy during all experiments with caged sentinel mosquitoes, and during Experiments 1 and 2 with pretreatment, treatment, and posttreatment measurements of mosquito abundance in CO2 traps. Downwind monarch larval and adult mortality were higher than upwind or control mortality up to 120 m, but not 170 m, from the spray path. In 1 experiment, monarchs exposed to spray as larvae developed into smaller adults, suggesting sublethal impacts. Milkweed host plants sprayed 1, but not 2 or 4 days previously, resulted in increased monarch larval mortality. Sentinel mosquito mortality was generally high, and CO2 traps revealed substantially lower mosquito abundance immediately after the treatment (>90% reduction) but <20% reduction 24 h after treatment. Our results suggest that ULV resmethrin applications will impact lepidopteran larvae and adults that are directly exposed to the spray but that generalizations about other nontarget taxa will require additional research. The magnitude of population-level impacts on monarchs will depend on the proportion of the population that is exposed.